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Neuronal oscillations enhance stimulus discrimination by ensuring action potential precision.

ABSTRACT: Although oscillations in membrane potential are a prominent feature of sensory, motor, and cognitive function, their precise role in signal processing remains elusive. Here we show, using a combination of in vivo, in vitro, and theoretical approaches, that both synaptically and intrinsically generated membrane potential oscillations dramatically improve action potential (AP) precision by removing the membrane potential variance associated with jitter-accumulating trains of APs. This increased AP precision occurred irrespective of cell type and--at oscillation frequencies ranging from 3 to 65 Hz--permitted accurate discernment of up to 1,000 different stimuli. At low oscillation frequencies, stimulus discrimination showed a clear phase dependence whereby inputs arriving during the trough and the early rising phase of an oscillation cycle were most robustly discriminated. Thus, by ensuring AP precision, membrane potential oscillations dramatically enhance the discriminatory capabilities of individual neurons and networks of cells and provide one attractive explanation for their abundance in neurophysiological systems.

SUBMITTER: Schaefer AT

PROVIDER: S-EPMC1459879 | biostudies-literature | 2006 Jun

REPOSITORIES: biostudies-literature

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Neuronal oscillations enhance stimulus discrimination by ensuring action potential precision.

Schaefer Andreas T AT Angelo Kamilla K Spors Hartwig H Margrie Troy W TW

PLoS biology 20060516 6

Although oscillations in membrane potential are a prominent feature of sensory, motor, and cognitive function, their precise role in signal processing remains elusive. Here we show, using a combination of in vivo, in vitro, and theoretical approaches, that both synaptically and intrinsically generated membrane potential oscillations dramatically improve action potential (AP) precision by removing the membrane potential variance associated with jitter-accumulating trains of APs. This increased AP ...[more]

PMID: 16689623

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Project description:ObjectivePrevious research from our laboratory comparing electrically evoked compound action potential (ECAP) artifact reduction methods has shown larger amplitudes and lower thresholds with cathodic-leading forward masking (CathFM) than with alternating polarity (AltPol). One interpretation of this result is that the anodic-leading phase used with AltPol elicits a less excitatory response (in contrast to results from recent studies with humans), which when averaged with responses to cathodic-leading stimuli, results in smaller amplitudes. Another interpretation is that the latencies of the responses to anodic- and cathodic-leading pulses differ, which when averaged together, result in smaller amplitudes than for either polarity alone due to temporal smearing. The purpose of this study was to separate the effects of stimulus polarity and artifact reduction method to determine the relative effects of each.DesignThis study used a within-subjects design. ECAP growth functions were obtained using CathFM, anodic-leading forward masking (AnodFM), and AltPol for 23 CI recipients (N = 13 Cochlear and N = 10 Advanced Bionics). N1 latency, amplitude, slope of the amplitude growth function, and threshold were compared across methods. Data were analyzed separately for each manufacturer due to inherent differences between devices.ResultsN1 latencies were significantly shorter for AnodFM than for CathFM and AltPol for both Cochlear and Advanced Bionics participants. Amplitudes were larger for AnodFM than for either CathFM or AltPol for Cochlear recipients; amplitude was not significantly different across methods for Advanced Bionics recipients. Slopes were shallowest for CathFM for Cochlear subjects, but were not significantly different among methods for Advanced Bionics subjects. Thresholds with AltPol were significantly higher than both FM methods for Cochlear recipients; there was no difference in threshold across methods for the Advanced Bionics recipients.ConclusionsFor Cochlear devices, the smaller amplitudes and higher thresholds observed for AltPol seem to be the result of latency differences between polarities. These results suggest that AltPol is not ideal for managing stimulus artifact for ECAP recordings. For the Advanced Bionics group, there were no significant differences among methods for amplitude, slope, or threshold, which suggests that polarity and artifact reduction method have little influence in these devices. We postulate that polarity effects are minimized for symmetrical biphasic pulses that lack an interphase gap, such as those used with Advanced Bionics devices; however, this requires further investigation.

Dataset Information

Neuronal oscillations enhance stimulus discrimination by ensuring action potential precision.

Publications

Neuronal oscillations enhance stimulus discrimination by ensuring action potential precision.

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