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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 transmission in isolated FFNs (, , ) with linear (a–c) and nonlinear (d–f) dendritic interactions.For each dendritic interaction type, raster plots for two different coupling strengths  are shown. Panels (a), (b), (d) and (e) display the network activity in the absence of oscillations; in panels (c) and (f) balanced oscillatory input is present (parameters see inset). The stimulation frequency  equals the propagation frequency  of the stable propagation shown in (a) and (d).
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pcbi-1003940-g001: Signal transmission in isolated FFNs (, , ) with linear (a–c) and nonlinear (d–f) dendritic interactions.For each dendritic interaction type, raster plots for two different coupling strengths are shown. Panels (a), (b), (d) and (e) display the network activity in the absence of oscillations; in panels (c) and (f) balanced oscillatory input is present (parameters see inset). The stimulation frequency equals the propagation frequency of the stable propagation shown in (a) and (d).

Mentions: Synchrony propagation through feed-forward structures has been demonstrated for additive and non-additive coupling, and non-oscillatory network background activity [21], [22], [25], [27], [28], [30]. In general, if synaptic coupling is additive (i.e., in the absence of dendritic spikes), the connection strength within the structure, i.e., synaptic efficiencies and/or connectivity, need to be much stronger (perhaps outside the biological plausible range) than for non-additive coupling (cf. Fig. 1a,d and [30], [31]). With too small coupling strength a synchronous signal fails to propagate, the synchronous activity dies out after a small number of layers (Fig. 1b,e).


Oscillation-induced signal transmission and gating in neural circuits.

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

Signal transmission in isolated FFNs (, , ) with linear (a–c) and nonlinear (d–f) dendritic interactions.For each dendritic interaction type, raster plots for two different coupling strengths  are shown. Panels (a), (b), (d) and (e) display the network activity in the absence of oscillations; in panels (c) and (f) balanced oscillatory input is present (parameters see inset). The stimulation frequency  equals the propagation frequency  of the stable propagation shown in (a) and (d).
© Copyright Policy
Related In: Results  -  Collection

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

pcbi-1003940-g001: Signal transmission in isolated FFNs (, , ) with linear (a–c) and nonlinear (d–f) dendritic interactions.For each dendritic interaction type, raster plots for two different coupling strengths are shown. Panels (a), (b), (d) and (e) display the network activity in the absence of oscillations; in panels (c) and (f) balanced oscillatory input is present (parameters see inset). The stimulation frequency equals the propagation frequency of the stable propagation shown in (a) and (d).
Mentions: Synchrony propagation through feed-forward structures has been demonstrated for additive and non-additive coupling, and non-oscillatory network background activity [21], [22], [25], [27], [28], [30]. In general, if synaptic coupling is additive (i.e., in the absence of dendritic spikes), the connection strength within the structure, i.e., synaptic efficiencies and/or connectivity, need to be much stronger (perhaps outside the biological plausible range) than for non-additive coupling (cf. Fig. 1a,d and [30], [31]). With too small coupling strength a synchronous signal fails to propagate, the synchronous activity dies out after a small number of layers (Fig. 1b,e).

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