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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 hippocampal-like networks.(a) Probability density function for delay distributions of neurons on a quadratic patch with side length . The conduction delay is composed of the distance-dependent axonal delay and the uniformly distributed dendritic delay (for details see Equations (12) – (15) and explaining text). (b) The panel shows up to which layer a synchronous pulse propagates along an FFN with the delay distribution taken from (a) in the presence of balanced oscillations for different patch sizes . The network setup is the same as in Fig. 9. With increasing patch size , and thus increasing connection lengths, the resonance frequencies are shifted to lower values. For further discussion see text.
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pcbi-1003940-g011: Signal propagation in hippocampal-like networks.(a) Probability density function for delay distributions of neurons on a quadratic patch with side length . The conduction delay is composed of the distance-dependent axonal delay and the uniformly distributed dendritic delay (for details see Equations (12) – (15) and explaining text). (b) The panel shows up to which layer a synchronous pulse propagates along an FFN with the delay distribution taken from (a) in the presence of balanced oscillations for different patch sizes . The network setup is the same as in Fig. 9. With increasing patch size , and thus increasing connection lengths, the resonance frequencies are shifted to lower values. For further discussion see text.

Mentions: In Fig. 11a we show the resulting probability density functions for different patch sizes . With increasing side length the probability distributions become broader and the peak of the distribution is shifted to larger delays. As shown in Fig. 11b synchronous pulses may propagate in FFNs in the presence of external oscillations. We observe resonances as before (cf. Fig. 6), and the resonance frequencies are shifted to smaller frequencies with increasing patch size .


Oscillation-induced signal transmission and gating in neural circuits.

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

Signal propagation in hippocampal-like networks.(a) Probability density function for delay distributions of neurons on a quadratic patch with side length . The conduction delay is composed of the distance-dependent axonal delay and the uniformly distributed dendritic delay (for details see Equations (12) – (15) and explaining text). (b) The panel shows up to which layer a synchronous pulse propagates along an FFN with the delay distribution taken from (a) in the presence of balanced oscillations for different patch sizes . The network setup is the same as in Fig. 9. With increasing patch size , and thus increasing connection lengths, the resonance frequencies are shifted to lower values. For further discussion see text.
© Copyright Policy
Related In: Results  -  Collection

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

pcbi-1003940-g011: Signal propagation in hippocampal-like networks.(a) Probability density function for delay distributions of neurons on a quadratic patch with side length . The conduction delay is composed of the distance-dependent axonal delay and the uniformly distributed dendritic delay (for details see Equations (12) – (15) and explaining text). (b) The panel shows up to which layer a synchronous pulse propagates along an FFN with the delay distribution taken from (a) in the presence of balanced oscillations for different patch sizes . The network setup is the same as in Fig. 9. With increasing patch size , and thus increasing connection lengths, the resonance frequencies are shifted to lower values. For further discussion see text.
Mentions: In Fig. 11a we show the resulting probability density functions for different patch sizes . With increasing side length the probability distributions become broader and the peak of the distribution is shifted to larger delays. As shown in Fig. 11b synchronous pulses may propagate in FFNs in the presence of external oscillations. We observe resonances as before (cf. Fig. 6), and the resonance frequencies are shifted to smaller frequencies with increasing patch size .

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