Abstract

Spike-timing-dependent plasticity (STDP) has been well established between excitatory neurons and several computational functions have been proposed in various neural systems. Despite some recent efforts, however, there is a significant lack of functional understanding of inhibitory STDP (iSTDP) and its interplay with excitatory STDP (eSTDP). Here, we demonstrate by analytical and numerical methods that iSTDP contributes crucially to the balance of excitatory and inhibitory weights for the selection of a specific signaling pathway among other pathways in a feedforward circuit. This pathway selection is based on the high sensitivity of STDP to correlations in spike times, which complements a recent proposal for the role of iSTDP in firing-rate based selection. Our model predicts that asymmetric anti-Hebbian iSTDP exceeds asymmetric Hebbian iSTDP for supporting pathway-specific balance, which we show is useful for propagating transient neuronal responses. Furthermore, we demonstrate how STDPs at excitatory–excitatory, excitatory–inhibitory, and inhibitory–excitatory synapses cooperate to improve the pathway selection. We propose that iSTDP is crucial for shaping the network structure that achieves efficient processing of synchronous spikes.

Highlights

  • Activity-dependent plasticity of synaptic connections between neurons is crucial for cortical circuit development and memory (Böhme et al, 1993; Hensch et al, 1998)

  • An extensive body of theoretical work has uncovered many interesting properties of excitatory Spike-timing-dependent plasticity (STDP): it can select input pathways based on their spike-time correlation (Kempter et al, 1999; Song et al, 2000; Gjorgjieva et al, 2011), it can generate a stable distribution of weights, it can perform selection of phase-locking in population firing (Gerstner et al, 1996; Senn and Buchs, 2003), it favors the emergence of functional neuronal assemblies (Izhikevich et al, 2004; Clopath et al, 2010), it stabilizes slow oscillations in recurrent networks (Kang et al, 2008) and it allows for rewiring of connections in the developing visual cortex (Song and Abbott, 2001; Senn and Buchs, 2003; Young et al, 2007)

  • Since there is no current consensus about a single type of inhibitory STDP (iSTDP) (Woodin et al, 2003; Haas et al, 2006; Kodangattil et al, 2013), this comparison allows us to link the shape of iSTDP learning windows to their functional implications

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Summary

Introduction

Activity-dependent plasticity of synaptic connections between neurons is crucial for cortical circuit development and memory (Böhme et al, 1993; Hensch et al, 1998). An extensive body of theoretical work has uncovered many interesting properties of excitatory STDP (eSTDP): it can select input pathways based on their spike-time correlation (Kempter et al, 1999; Song et al, 2000; Gjorgjieva et al, 2011), it can generate a stable distribution of weights (van Rossum et al, 2000; Gütig et al, 2003; Gilson and Fukai, 2011), it can perform selection of phase-locking in population firing (Gerstner et al, 1996; Senn and Buchs, 2003), it favors the emergence of functional neuronal assemblies (Izhikevich et al, 2004; Clopath et al, 2010), it stabilizes slow oscillations in recurrent networks (Kang et al, 2008) and it allows for rewiring of connections in the developing visual cortex (Song and Abbott, 2001; Senn and Buchs, 2003; Young et al, 2007). Neither experimental nor theoretical approaches provide a consensus for the shape of the iSTDP learning window, in contrast to eSTDP for which the temporally Hebbian nature (LTP for pre-post pairing, LTD for postpre pairing) is observed and addressed in the vast majority of cases

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