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Spiking neurons that keep the rhythm

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Abstract

Detecting the temporal relationship among events in the environment is a fundamental goal of the brain. Following pulses of rhythmic stimuli, neurons of the retina and cortex produce activity that closely approximates the timing of an omitted pulse. This omitted stimulus response (OSR) is generally interpreted as a transient response to rhythmic input and is thought to form a basis of short-term perceptual memories. Despite its ubiquity across species and experimental protocols, the mechanisms underlying OSRs remain poorly understood. In particular, the highly transient nature of OSRs, typically limited to a single cycle after stimulation, cannot be explained by a simple mechanism that would remain locked to the frequency of stimulation. Here, we describe a set of realistic simulations that capture OSRs over a range of stimulation frequencies matching experimental work. The model does not require an explicit mechanism for learning temporal sequences. Instead, it relies on spike timing-dependent plasticity (STDP), a form of synaptic modification that is sensitive to the timing of pre- and post-synaptic action potentials. In the model, the transient nature of OSRs is attributed to the heterogeneous nature of neural properties and connections, creating intricate forms of activity that are continuously changing over time. Combined with STDP, neural heterogeneity enabled OSRs to complex rhythmic patterns as well as OSRs following a delay period. These results link the response of neurons to rhythmic patterns with the capacity of heterogeneous circuits to produce transient and highly flexible forms of neural activity.

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Acknowledgments

JPT is supported by postdoctoral fellowships from the Natural Sciences and Engineering Research Council of Canada and the Fonds de Recherche en Santé du Québec. PC is supported by grants from the Natural Sciences and Engineering Research Council of Canada and the Fonds de Recherche en Santé du Québec (infrastructure grant).

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Authors and Affiliations

  1. Department of Psychological and Brain Sciences, Indiana University, 1101 East Tenth Street, Bloomington, IN, 47405, USA

    Jean-Philippe Thivierge

  2. Groupe de Recherche sur le Système Nerveux Central, Département de Physiologie, Université de Montréal, Montreal, QC, Canada, H3T 1J4

    Paul Cisek

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  1. Jean-Philippe Thivierge
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Correspondence to Jean-Philippe Thivierge.

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Thivierge, JP., Cisek, P. Spiking neurons that keep the rhythm. J Comput Neurosci 30, 589–605 (2011). https://doi.org/10.1007/s10827-010-0280-1

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