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Oscillation-induced signal transmission and gating in neural circuits.

Jahnke S, Memmesheimer RM, Timme M - PLoS Comput. Biol. (2014)

Bottom Line: We find that for standard, additive couplings and a net excitatory effect of oscillations, robust propagation of synchrony is enabled in less prominent feed-forward structures than in systems without oscillations.Our results are of particular interest for the interpretation of sharp wave/ripple complexes in the hippocampus, where previously learned spike patterns are replayed in conjunction with global high-frequency oscillations.We suggest that the oscillations may serve to stabilize the replay.

View Article: PubMed Central - PubMed

Affiliation: Network Dynamics, Max Planck Institute for Dynamics and Self-Organization (MPIDS), Göttingen, Germany; Bernstein Center for Computational Neuroscience (BCCN), Göttingen, Germany; Institute for Nonlinear Dynamics, Fakultät für Physik, Georg-August Universität Göttingen, Göttingen Germany.

ABSTRACT
Reliable signal transmission constitutes a key requirement for neural circuit function. The propagation of synchronous pulse packets through recurrent circuits is hypothesized to be one robust form of signal transmission and has been extensively studied in computational and theoretical works. Yet, although external or internally generated oscillations are ubiquitous across neural systems, their influence on such signal propagation is unclear. Here we systematically investigate the impact of oscillations on propagating synchrony. We find that for standard, additive couplings and a net excitatory effect of oscillations, robust propagation of synchrony is enabled in less prominent feed-forward structures than in systems without oscillations. In the presence of non-additive coupling (as mediated by fast dendritic spikes), even balanced oscillatory inputs may enable robust propagation. Here, emerging resonances create complex locking patterns between oscillations and spike synchrony. Interestingly, these resonances make the circuits capable of selecting specific pathways for signal transmission. Oscillations may thus promote reliable transmission and, in co-action with dendritic nonlinearities, provide a mechanism for information processing by selectively gating and routing of signals. Our results are of particular interest for the interpretation of sharp wave/ripple complexes in the hippocampus, where previously learned spike patterns are replayed in conjunction with global high-frequency oscillations. We suggest that the oscillations may serve to stabilize the replay.

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Signal propagation in FFNs with broad delay distribution.(a) Probability density function (10) of log-normal delay distribution with mode ms and different standard deviations  (cf. also Equation 11). (b) The panel shows up to which layer a synchronous pulse propagates in the presence (solid lines) and in the absence (dashed lines) of balanced oscillations for different layer sizes  (color code). The network setup is the same as in Fig. 4 (, , nS; with external oscillation parameters: , nS, nS, nS, , Hz). With increasing width of the delay distribution, the inputs from one layer to the following layer become more and more desynchronized, and thus signals propagate over fewer and fewer layers. However, by increasing the layer size oscillation-induced signal propagation is possible, even for very broad delay distributions. For further explanation see text.
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pcbi-1003940-g009: Signal propagation in FFNs with broad delay distribution.(a) Probability density function (10) of log-normal delay distribution with mode ms and different standard deviations (cf. also Equation 11). (b) The panel shows up to which layer a synchronous pulse propagates in the presence (solid lines) and in the absence (dashed lines) of balanced oscillations for different layer sizes (color code). The network setup is the same as in Fig. 4 (, , nS; with external oscillation parameters: , nS, nS, nS, , Hz). With increasing width of the delay distribution, the inputs from one layer to the following layer become more and more desynchronized, and thus signals propagate over fewer and fewer layers. However, by increasing the layer size oscillation-induced signal propagation is possible, even for very broad delay distributions. For further explanation see text.

Mentions: In Fig. 9a we show the log-normal distribution for fixed and different and .


Oscillation-induced signal transmission and gating in neural circuits.

Jahnke S, Memmesheimer RM, Timme M - PLoS Comput. Biol. (2014)

Signal propagation in FFNs with broad delay distribution.(a) Probability density function (10) of log-normal delay distribution with mode ms and different standard deviations  (cf. also Equation 11). (b) The panel shows up to which layer a synchronous pulse propagates in the presence (solid lines) and in the absence (dashed lines) of balanced oscillations for different layer sizes  (color code). The network setup is the same as in Fig. 4 (, , nS; with external oscillation parameters: , nS, nS, nS, , Hz). With increasing width of the delay distribution, the inputs from one layer to the following layer become more and more desynchronized, and thus signals propagate over fewer and fewer layers. However, by increasing the layer size oscillation-induced signal propagation is possible, even for very broad delay distributions. For further explanation see text.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4263355&req=5

pcbi-1003940-g009: Signal propagation in FFNs with broad delay distribution.(a) Probability density function (10) of log-normal delay distribution with mode ms and different standard deviations (cf. also Equation 11). (b) The panel shows up to which layer a synchronous pulse propagates in the presence (solid lines) and in the absence (dashed lines) of balanced oscillations for different layer sizes (color code). The network setup is the same as in Fig. 4 (, , nS; with external oscillation parameters: , nS, nS, nS, , Hz). With increasing width of the delay distribution, the inputs from one layer to the following layer become more and more desynchronized, and thus signals propagate over fewer and fewer layers. However, by increasing the layer size oscillation-induced signal propagation is possible, even for very broad delay distributions. For further explanation see text.
Mentions: In Fig. 9a we show the log-normal distribution for fixed and different and .

Bottom Line: We find that for standard, additive couplings and a net excitatory effect of oscillations, robust propagation of synchrony is enabled in less prominent feed-forward structures than in systems without oscillations.Our results are of particular interest for the interpretation of sharp wave/ripple complexes in the hippocampus, where previously learned spike patterns are replayed in conjunction with global high-frequency oscillations.We suggest that the oscillations may serve to stabilize the replay.

View Article: PubMed Central - PubMed

Affiliation: Network Dynamics, Max Planck Institute for Dynamics and Self-Organization (MPIDS), Göttingen, Germany; Bernstein Center for Computational Neuroscience (BCCN), Göttingen, Germany; Institute for Nonlinear Dynamics, Fakultät für Physik, Georg-August Universität Göttingen, Göttingen Germany.

ABSTRACT
Reliable signal transmission constitutes a key requirement for neural circuit function. The propagation of synchronous pulse packets through recurrent circuits is hypothesized to be one robust form of signal transmission and has been extensively studied in computational and theoretical works. Yet, although external or internally generated oscillations are ubiquitous across neural systems, their influence on such signal propagation is unclear. Here we systematically investigate the impact of oscillations on propagating synchrony. We find that for standard, additive couplings and a net excitatory effect of oscillations, robust propagation of synchrony is enabled in less prominent feed-forward structures than in systems without oscillations. In the presence of non-additive coupling (as mediated by fast dendritic spikes), even balanced oscillatory inputs may enable robust propagation. Here, emerging resonances create complex locking patterns between oscillations and spike synchrony. Interestingly, these resonances make the circuits capable of selecting specific pathways for signal transmission. Oscillations may thus promote reliable transmission and, in co-action with dendritic nonlinearities, provide a mechanism for information processing by selectively gating and routing of signals. Our results are of particular interest for the interpretation of sharp wave/ripple complexes in the hippocampus, where previously learned spike patterns are replayed in conjunction with global high-frequency oscillations. We suggest that the oscillations may serve to stabilize the replay.

Show MeSH
Related in: MedlinePlus