GABA inhibition modulates NMDA-R mediated spike timing dependent plasticity (STDP) in a biophysical model
Abstract
Spike timing dependent plasticity (STDP) has been demonstrated in various neural systems of many animals. It has been shown that STDP depends on the target and the location of the synapse and is dynamically regulated by the activity of adjacent synapses, the presence of postsynaptic calcium, presynaptic GABA inhibition or the action of neuromodulators. Recent experimental evidence has reported that the profile of STDP in the CA1 pyramidal neuron can be classified into two types depending on its dendritic location: (1) A symmetric STDP profile in the proximal to the soma dendrites, and (2) an asymmetric one in the distal dendrites. Bicuculline application revealed that GABA"A is responsible for the symmetry of the STDP curve. We investigate via computer simulations how GABA"A shapes the STDP profile in the CA1 pyramidal neuron dendrites when it is driven by excitatory spike pairs (doublets). The model constructed uses calcium as the postsynaptic signaling agent for STDP and is shown to be consistent with classical long-term potentiation (LTP) and long-term depression (LTD) induced by several doublet stimulation paradigms in the absence of inhibition. Overall, simulation results provide computational evidence for the first time that the switch between the symmetrical and the asymmetrical STDP operational modes is indeed due to GABA inhibition. Furthermore, gamma frequency inhibition and not theta one is responsible for the transition from asymmetry-to-symmetry. The resulted symmetrical STDP profile is centered at +10 ms with two distinct LTD tails at -10 and +40 ms. Finally, the asymmetry-to-symmetry transition is strongly dependent on the strength (conductance) of inhibition and its relative onset with respect to pre- and postsynaptic spike stimulation.
References
[1]
The relation between spike-timing dependent plasticity and Ca2+ dynamics in the hippocampal CA1 network. Neuroscience. v145. 80-87.
[2]
Synaptic plasticity in a cerebellum-like structure depends on temporal order. Nature. v387. 278-281.
[3]
Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. Journal of Neuroscience. v18. 10464-10472.
[4]
Timing in synaptic plasticity: from detection to integration. TINS. v28 i5. 222-228.
[5]
Spike timing dependent plasticity: a Hebbian learning rule. Annual Review of Neuroscience. v31. 25-46.
[6]
Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature. v378. 75-78.
[7]
Frequency of gamma oscillations routes flows of information in the hippocampus. Nature. v462. 353-357.
[8]
Encoding and retrieval in a CA1 microcircuit model of the hippocampus. In: Kurkova, V., Neruda, R., Koutnik, J. (Eds.), LNCS, Vol. 5164. Springer-Verlag, Berlin, Heidelberg. pp. 238-247.
[9]
Modelling the STDP symmetry-to-asymmetry transition in the presence of GABAergic inhibition. Neural Network World. v19 i5. 471-481.
[10]
Encoding and retrieval in the hippocampal CA1 microcircuit model. Hippocampus. v20 i3. 423-446.
[11]
Hippocampus, microcircuits and associative memory. Neural Networks. v22 i8. 1120-1128.
[12]
Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures. Journal of Physiology. v507. 237-247.
[13]
Forward and reverse hippocampal place-cell sequences during ripples. Nature Neuroscience. v10 i10. 1241-1242.
[14]
Simulating, analyzing and animating dynamical systems. SIAM, Philadelphia.
[15]
Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature. v440. 680-683.
[16]
Spike-timing-dependent synaptic plasticity depends on dendritic location. Nature. v434 i7030. 221-225.
[17]
Dynamics of storage and recall in hippocampal associative memory networks. In: Erdi, P., Esposito, A., Marinaro, M., Scarpetta, S. (Eds.), Computational neuroscience: cortical dynamics, Springer-Verlag, Berlin, Heidelberg. pp. 1-23.
[18]
Dynamical information processing in the CA1 microcircuit of the hippocampus. In: Computational modeling in behavioral neuroscience: closing the gap between neurophysiology and behavior, Psychology Press, Taylor and Francis Group, London.
[19]
A proposed function of the hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neural Computation. v14. 793-817.
[20]
Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: computational modelling and brain slice physiology. Journal of Neuroscience. v14. 3898-3914.
[21]
Locally dynamic synaptic learning rules in pyramidal neuron dendrites. Nature. v450 i7173. 1195-1200.
[22]
LTD windows of the STDP learning rule and synaptic connections having a large transmission delay enable robust sequence learning amid background noise. Cognitive Neurodynamics. v3. 119-130.
[23]
Dorsal hippocampus, CA3 and CA1 lesions disrupt temporal sequence completion. Behavioral Neuroscience. v122. 9-15.
[24]
Interneurons of the dentate gyrus: an overview of cell types, terminal fields and neurochemical identity. Progress in Brain Research. v163. 217-232.
[25]
Dissociation of the medial and lateral perforant path projections into dorsal DG, CA3, and CA1 for spatial and nonspatial (visual object) information processing. Behavioral Neuroscience. v121. 742-750.
[26]
Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science. v321. 53-57.
[27]
Differential contribution of NMDA receptors in hippocampal subregions to spatial working memory. Nature Neuroscience. v5. 162-168.
[28]
Differential contributions of dorsal hippocampal subregions to memory acquisition and retrieval in contextual-fear conditioning. Hippocampus. v14. 301-310.
[29]
Learning rules for spike timing-dependent plasticity depend on dendritic synapse location. Journal of Neuroscience. v26 i41. 10420-10429.
[30]
Entorhinal inputs to hippocampal CA1 and dentate gyrus in the rat: a current-source-density study. J. Neurophys. v73 i6. 2392-2403.
[31]
A synaptically controlled, associative signal for hebbian plasticity in hippocampal neurons. Science. v275. 209-213.
[32]
Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science. v275. 213-215.
[33]
Modelling the dentate gyrus. Progress in Brain Research. v163. 639-658.
[34]
Calcium stores regulate the polarity and input specificity of synaptic modification. Nature. v408. 584-588.
[35]
Hippocampal conjuctive encoding, storage, and recall: avoiding a trade-off. Hippocampus. v4. 661-682.
[36]
Neural networks in the brain involved in memory and recall. Progress in Brain Research. v102. 335-341.
[37]
Calcium time course as a signal for spike-timing-dependent plasticity. Journal of Neurophysiology. v93. 2600-2613.
[38]
Neuromodulators control the polarity of spike-timing-dependent synaptic plasticity. Neuron. v55 i6. 919-929.
[39]
Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron. v32. 1149-1164.
[40]
Conduction latency along CA3 hippocampal axons from rat. Hippocampus. v13. 953-961.
[41]
Computational constraints between retrieving the past and predicting the future, and the CA3-CA1 differentiation. Hippocampus. v14. 539-556.
[42]
Spatial analysis of spike-timing-dependent LTP and LTD in the CA1 area of hippocampal slices using optical imaging. Hippocampus. v15. 104-109.
[43]
Cell-specific, spike timing-dependent plasticities in the dorsal cochlear nucleus. Nature Neuroscience. v7 i7. 719-725.
[44]
Hippocampus as a comparator: role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus. v11. 578-598.
[45]
Coactivation and timing-dependent integration of synaptic potentiation and depression. Nature Neuroscience. v8 i2. 187-193.
[46]
Networks of interneurons with fast and slow gamma-aminobutyric acid type A (GABAA) kinetics provide substrate for mixed gamma-theta rhythm. Proceedings of the National Academy of Sciences. v97 i10. 8128-8133.
[47]
Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature. v373. 612-615.
[48]
Stimulus timing-dependent plasticity in cortical processing of orientation. Neuron. v32. 315-323.
[49]
Feedforward excitation of the hippocampus by afferents from the entorhinal cortex: redefinition of the role of the trisynaptic pathway. Proceedings of the National Academy of Sciences. v87. 5832-5836.
[50]
A critical window for cooperation and competition among developing retinotectal synapses. Nature. v395. 37-44.
- GABA inhibition modulates NMDA-R mediated spike timing dependent plasticity (STDP) in a biophysical model
Recommendations
How Bursts Shape the STDP Curve in the Presence/Absence of GABAergic Inhibition
ICANN '09: Proceedings of the 19th International Conference on Artificial Neural Networks: Part IIt has been known for some time that the synapses of the CA1 pyramidal cells are surprisingly unreliable at signalling the arrival of single spikes to the postsynaptic neuron [2]. On the other hand, bursts of spikes are reliably signalled, because ...
Action potential bursts modulate the NMDA-R mediated spike timing dependent plasticity in a biophysical model
ICANN'10: Proceedings of the 20th international conference on Artificial neural networks: Part ISpike timing dependent plasticity (STDP) requires the temporal association of presynaptic and postsynaptic action potentials (APs). However, some synapses in the CA1 region of the hippocampus are suprisingle unreliable at signaling the arrival of single ...
Interplay of the magnitude and time-course of postsynaptic Ca2+ concentration in producing spike timing-dependent plasticity
Synaptic strength can be modified by the relative timing of pre- and postsynaptic activity, a phenomenon termed spike timing-dependent plasticity (STDP). Studies of neurons in the hippocampus and in other regions have found that when presynaptic ...
Comments
Please enable JavaScript to view thecomments powered by Disqus.Information & Contributors
Information
Published In
Copyright © Elsevier Ltd © 2010.
Publisher
Elsevier Science Ltd.
United Kingdom
Publication History
Published: 01 January 2011
Author Tags
Qualifiers
- Article
Contributors
Other Metrics
Bibliometrics & Citations
Bibliometrics
Article Metrics
- 0Total Citations
- 0Total Downloads
- Downloads (Last 12 months)0
- Downloads (Last 6 weeks)0
Reflects downloads up to 26 Dec 2024