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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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Related in: MedlinePlus

Resonances in FFNs with broad delay distribution (same network setup as in Fig. 9).The panels show until which layer a synchronous pulse successfully propagate versus the stimulation frequency . In (a) the layer size is fixed () and the width  of the delay distribution is varied. Here, for heterogeneous coupling delays (orange) a synchronous signal propagates for all stimulation frequencies (and even in the absence of external stimulations). With increasing  the fraction of frequencies for which a robust signal propagation is possible decreases, and for sufficiently large  no robust signal propagation is possible anymore (red). In (b) the width of the delay distribution is fixed (ms) and the layer size  is varied. Here, for small  robust signal propagation is not possible (independent of the stimulation frequency), however, with increasing layer size the fraction of stimulation frequencies which enable a robust signal propagation increases. For further explanation see text.
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pcbi-1003940-g010: Resonances in FFNs with broad delay distribution (same network setup as in Fig. 9).The panels show until which layer a synchronous pulse successfully propagate versus the stimulation frequency . In (a) the layer size is fixed () and the width of the delay distribution is varied. Here, for heterogeneous coupling delays (orange) a synchronous signal propagates for all stimulation frequencies (and even in the absence of external stimulations). With increasing the fraction of frequencies for which a robust signal propagation is possible decreases, and for sufficiently large no robust signal propagation is possible anymore (red). In (b) the width of the delay distribution is fixed (ms) and the layer size is varied. Here, for small robust signal propagation is not possible (independent of the stimulation frequency), however, with increasing layer size the fraction of stimulation frequencies which enable a robust signal propagation increases. For further explanation see text.

Mentions: We illustrate the effect of an increasing width of delay distribution in Fig. 10a: Starting with a setup where a synchronous signal can propagate over all layers for homogeneous coupling even in the absence of external oscillations, an increase of the width of the delay distribution results in the formation of resonance peaks. The arriving inputs become more and more distributed and therefore signal propagation is only possible if the input from the previous layer is supported by external oscillations. If the delay distribution becomes broader, the frequency bands which enable oscillation-induced signal transmission become narrower, and eventually for sufficiently large a robust signal transmission is not possible anymore.


Oscillation-induced signal transmission and gating in neural circuits.

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

Resonances in FFNs with broad delay distribution (same network setup as in Fig. 9).The panels show until which layer a synchronous pulse successfully propagate versus the stimulation frequency . In (a) the layer size is fixed () and the width  of the delay distribution is varied. Here, for heterogeneous coupling delays (orange) a synchronous signal propagates for all stimulation frequencies (and even in the absence of external stimulations). With increasing  the fraction of frequencies for which a robust signal propagation is possible decreases, and for sufficiently large  no robust signal propagation is possible anymore (red). In (b) the width of the delay distribution is fixed (ms) and the layer size  is varied. Here, for small  robust signal propagation is not possible (independent of the stimulation frequency), however, with increasing layer size the fraction of stimulation frequencies which enable a robust signal propagation increases. For further explanation see text.
© Copyright Policy
Related In: Results  -  Collection

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

pcbi-1003940-g010: Resonances in FFNs with broad delay distribution (same network setup as in Fig. 9).The panels show until which layer a synchronous pulse successfully propagate versus the stimulation frequency . In (a) the layer size is fixed () and the width of the delay distribution is varied. Here, for heterogeneous coupling delays (orange) a synchronous signal propagates for all stimulation frequencies (and even in the absence of external stimulations). With increasing the fraction of frequencies for which a robust signal propagation is possible decreases, and for sufficiently large no robust signal propagation is possible anymore (red). In (b) the width of the delay distribution is fixed (ms) and the layer size is varied. Here, for small robust signal propagation is not possible (independent of the stimulation frequency), however, with increasing layer size the fraction of stimulation frequencies which enable a robust signal propagation increases. For further explanation see text.
Mentions: We illustrate the effect of an increasing width of delay distribution in Fig. 10a: Starting with a setup where a synchronous signal can propagate over all layers for homogeneous coupling even in the absence of external oscillations, an increase of the width of the delay distribution results in the formation of resonance peaks. The arriving inputs become more and more distributed and therefore signal propagation is only possible if the input from the previous layer is supported by external oscillations. If the delay distribution becomes broader, the frequency bands which enable oscillation-induced signal transmission become narrower, and eventually for sufficiently large a robust signal transmission is not possible anymore.

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