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Self-motion evokes precise spike timing in the primate vestibular system.

ABSTRACT: The accurate representation of self-motion requires the efficient processing of sensory input by the vestibular system. Conventional wisdom is that vestibular information is exclusively transmitted through changes in firing rate, yet under this assumption vestibular neurons display relatively poor detection and information transmission. Here, we carry out an analysis of the system's coding capabilities by recording neuronal responses to repeated presentations of naturalistic stimuli. We find that afferents with greater intrinsic variability reliably discriminate between different stimulus waveforms through differential patterns of precise (?6?ms) spike timing, while those with minimal intrinsic variability do not. A simple mathematical model provides an explanation for this result. Postsynaptic central neurons also demonstrate precise spike timing, suggesting that higher brain areas also represent self-motion using temporally precise firing. These findings demonstrate that two distinct sensory channels represent vestibular information: one using rate coding and the other that takes advantage of precise spike timing.

SUBMITTER: Jamali M

PROVIDER: S-EPMC5095295 | biostudies-literature | 2016 Oct

REPOSITORIES: biostudies-literature

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Self-motion evokes precise spike timing in the primate vestibular system.

Jamali Mohsen M Chacron Maurice J MJ Cullen Kathleen E KE

Nature communications 20161027

The accurate representation of self-motion requires the efficient processing of sensory input by the vestibular system. Conventional wisdom is that vestibular information is exclusively transmitted through changes in firing rate, yet under this assumption vestibular neurons display relatively poor detection and information transmission. Here, we carry out an analysis of the system's coding capabilities by recording neuronal responses to repeated presentations of naturalistic stimuli. We find tha ...[more]

PMID: 27786265

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Project description:Classic in vitro studies have described spike-timing-dependent plasticity (STDP) at a synapse: the connection from neuron A to neuron B is strengthened (or weakened) when A fires before (or after) B within an optimal time window. Accordingly, more recent in vivo works have demonstrated behavioral effects consistent with an STDP mechanism; however, many relied on single-unit recordings. The ability to modify cortical connections becomes useful in the context of injury, when connectivity and associated behavior are compromised. To avoid the need for long-term, stable isolation of single units, one could control timed activation of two cortical sites with paired electrical stimulation. We tested the hypothesis that STDP could be induced via prolonged paired stimulation as quantified by cortical evoked potentials (EPs) in the sensorimotor cortex of awake, behaving monkeys. Paired simulation between two interconnected sites produced robust effects in EPs consistent with STDP, but only at 2/15 tested pairs. The stimulation protocol often produced increases in global network excitability or depression of the conditioned pair. Together, these results suggest that paired stimulation in vivo is a viable method to induce STDP between cortical populations, but that factors beyond activation timing must be considered to produce conditioning effects.SIGNIFICANCE STATEMENT Plasticity of neural connections is important for development, learning, memory, and recovery from injury. Cellular mechanisms underlying spike-timing-dependent plasticity have been studied extensively in vitro Recent in vivo work has demonstrated results consistent with the previously defined cellular mechanisms; however, the output measure in these studies was typically an indirect assessment of plasticity at the neural level. Here, we show direct plasticity in recordings of neuronal populations in awake, behaving nonhuman primates induced by paired electrical stimulation. In contrast to in vitro studies, we found that plastic effects were only produced between specific cortical areas. These findings suggest that similar mechanisms drive plasticity in vitro and in vivo, but that cortical architecture may contribute significantly to site-dependent effects.

Dataset Information

Self-motion evokes precise spike timing in the primate vestibular system.

Publications

Self-motion evokes precise spike timing in the primate vestibular system.

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