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      STDP Allows Close-to-Optimal Spatiotemporal Spike Pattern Detection by Single Coincidence Detector Neurons

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          Highlights

          • Repeating spike patterns exist and are informative. Can a single cell do the readout?

          • We show how a leaky integrate-and-fire (LIF) can do this readout optimally.

          • The optimal membrane time constant is short, possibly much shorter than the pattern.

          • Spike-timing-dependent plasticity (STDP) can turn a neuron into an optimal detector.

          • These results may explain how humans can learn repeating visual or auditory sequences.

          Abstract

          Repeating spatiotemporal spike patterns exist and carry information. How this information is extracted by downstream neurons is unclear. Here we theoretically investigate to what extent a single cell could detect a given spike pattern and what the optimal parameters to do so are, in particular the membrane time constant τ . Using a leaky integrate-and-fire (LIF) neuron with homogeneous Poisson input, we computed this optimum analytically. We found that a relatively small τ (at most a few tens of ms) is usually optimal, even when the pattern is much longer. This is somewhat counter-intuitive as the resulting detector ignores most of the pattern, due to its fast memory decay. Next, we wondered if spike-timing-dependent plasticity (STDP) could enable a neuron to reach the theoretical optimum. We simulated a LIF equipped with additive STDP, and repeatedly exposed it to a given input spike pattern. As in previous studies, the LIF progressively became selective to the repeating pattern with no supervision, even when the pattern was embedded in Poisson activity. Here we show that, using certain STDP parameters, the resulting pattern detector is optimal. These mechanisms may explain how humans learn repeating sensory sequences. Long sequences could be recognized thanks to coincidence detectors working at a much shorter timescale. This is consistent with the fact that recognition is still possible if a sound sequence is compressed, played backward, or scrambled using 10-ms bins. Coincidence detection is a simple yet powerful mechanism, which could be the main function of neurons in the brain.

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          Most cited references38

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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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            A review of the integrate-and-fire neuron model: I. Homogeneous synaptic input.

            A Burkitt (2006)
            The integrate-and-fire neuron model is one of the most widely used models for analyzing the behavior of neural systems. It describes the membrane potential of a neuron in terms of the synaptic inputs and the injected current that it receives. An action potential (spike) is generated when the membrane potential reaches a threshold, but the actual changes associated with the membrane voltage and conductances driving the action potential do not form part of the model. The synaptic inputs to the neuron are considered to be stochastic and are described as a temporally homogeneous Poisson process. Methods and results for both current synapses and conductance synapses are examined in the diffusion approximation, where the individual contributions to the postsynaptic potential are small. The focus of this review is upon the mathematical techniques that give the time distribution of output spikes, namely stochastic differential equations and the Fokker-Planck equation. The integrate-and-fire neuron model has become established as a canonical model for the description of spiking neurons because it is capable of being analyzed mathematically while at the same time being sufficiently complex to capture many of the essential features of neural processing. A number of variations of the model are discussed, together with the relationship with the Hodgkin-Huxley neuron model and the comparison with electrophysiological data. A brief overview is given of two issues in neural information processing that the integrate-and-fire neuron model has contributed to - the irregular nature of spiking in cortical neurons and neural gain modulation.
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              Stable Hebbian learning from spike timing-dependent plasticity.

              We explore a synaptic plasticity model that incorporates recent findings that potentiation and depression can be induced by precisely timed pairs of synaptic events and postsynaptic spikes. In addition we include the observation that strong synapses undergo relatively less potentiation than weak synapses, whereas depression is independent of synaptic strength. After random stimulation, the synaptic weights reach an equilibrium distribution which is stable, unimodal, and has positive skew. This weight distribution compares favorably to the distributions of quantal amplitudes and of receptor number observed experimentally in central neurons and contrasts to the distribution found in plasticity models without size-dependent potentiation. Also in contrast to those models, which show strong competition between the synapses, stable plasticity is achieved with little competition. Instead, competition can be introduced by including a separate mechanism that scales synaptic strengths multiplicatively as a function of postsynaptic activity. In this model, synaptic weights change in proportion to how correlated they are with other inputs onto the same postsynaptic neuron. These results indicate that stable correlation-based plasticity can be achieved without introducing competition, suggesting that plasticity and competition need not coexist in all circuits or at all developmental stages.
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                Author and article information

                Contributors
                Journal
                Neuroscience
                Neuroscience
                Neuroscience
                Elsevier Science
                0306-4522
                1873-7544
                01 October 2018
                01 October 2018
                : 389
                : 133-140
                Affiliations
                CERCO UMR5549 CNRS – Université Toulouse 3, France
                Article
                S0306-4522(17)30437-2
                10.1016/j.neuroscience.2017.06.032
                6372004
                28668487
                0ac3822c-ee12-4b44-aaf9-27f8994f94a7
                © 2017 The Author(s)

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 21 April 2017
                : 19 June 2017
                Categories
                Article

                Neurosciences
                ltd, long-term depression,ltp, long-term potentiation,lif, leaky integrate-and-fire,snr, signal-to-noise ratio,stdp, spike-timing-dependent plasticity,spike-timing-dependent plasticity (stdp),leaky integrate-and-fire neuron,coincidence detection,multi-neuron spike sequence,spatiotemporal spike pattern,unsupervised learning

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