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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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Activation of specific signal transmissions in FFNs with different resonance frequencies.(a) With increasing average coupling delays  (distribution width ms) resonance peaks (isolated FFN; , , , nS) are shifted to lower frequencies (cf. Equation 6). The panels show up to which layer a synchronous pulse propagates in the presence of balanced oscillations (, , nS, nS, ms). The width of the resonance peaks increases with increasing size of the dendritic integration window (solid: ms, dashed: ms, dotted: ms). (b) Raster plot of the spiking activity of a recurrent network (, , nS, nS) which contains two FFNs (, , nS) which share the initial layer. Both FFNs have different average coupling delays (ms and ms; ms) and thus different resonance frequencies (cf. panel a); for the remaining connections the average coupling delays is ms. Whereas a synchronous pulse extinguishes after a few layers in the absence of oscillations (ms), it may propagate along the layers of one FFN or the other depending on the stimulation frequency (ms and ms; , nS, nS, ms). Panel (c) is a close-up view of the raster plot shown in (b).
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pcbi-1003940-g008: Activation of specific signal transmissions in FFNs with different resonance frequencies.(a) With increasing average coupling delays (distribution width ms) resonance peaks (isolated FFN; , , , nS) are shifted to lower frequencies (cf. Equation 6). The panels show up to which layer a synchronous pulse propagates in the presence of balanced oscillations (, , nS, nS, ms). The width of the resonance peaks increases with increasing size of the dendritic integration window (solid: ms, dashed: ms, dotted: ms). (b) Raster plot of the spiking activity of a recurrent network (, , nS, nS) which contains two FFNs (, , nS) which share the initial layer. Both FFNs have different average coupling delays (ms and ms; ms) and thus different resonance frequencies (cf. panel a); for the remaining connections the average coupling delays is ms. Whereas a synchronous pulse extinguishes after a few layers in the absence of oscillations (ms), it may propagate along the layers of one FFN or the other depending on the stimulation frequency (ms and ms; , nS, nS, ms). Panel (c) is a close-up view of the raster plot shown in (b).

Mentions: We illustrate this dependency in Fig. 8a indicating the resonance peaks for different . Here, the coupling delays between neurons of successive layers are drawn uniformly from an interval of length centered at , (7)


Oscillation-induced signal transmission and gating in neural circuits.

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

Activation of specific signal transmissions in FFNs with different resonance frequencies.(a) With increasing average coupling delays  (distribution width ms) resonance peaks (isolated FFN; , , , nS) are shifted to lower frequencies (cf. Equation 6). The panels show up to which layer a synchronous pulse propagates in the presence of balanced oscillations (, , nS, nS, ms). The width of the resonance peaks increases with increasing size of the dendritic integration window (solid: ms, dashed: ms, dotted: ms). (b) Raster plot of the spiking activity of a recurrent network (, , nS, nS) which contains two FFNs (, , nS) which share the initial layer. Both FFNs have different average coupling delays (ms and ms; ms) and thus different resonance frequencies (cf. panel a); for the remaining connections the average coupling delays is ms. Whereas a synchronous pulse extinguishes after a few layers in the absence of oscillations (ms), it may propagate along the layers of one FFN or the other depending on the stimulation frequency (ms and ms; , nS, nS, ms). Panel (c) is a close-up view of the raster plot shown in (b).
© Copyright Policy
Related In: Results  -  Collection

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

pcbi-1003940-g008: Activation of specific signal transmissions in FFNs with different resonance frequencies.(a) With increasing average coupling delays (distribution width ms) resonance peaks (isolated FFN; , , , nS) are shifted to lower frequencies (cf. Equation 6). The panels show up to which layer a synchronous pulse propagates in the presence of balanced oscillations (, , nS, nS, ms). The width of the resonance peaks increases with increasing size of the dendritic integration window (solid: ms, dashed: ms, dotted: ms). (b) Raster plot of the spiking activity of a recurrent network (, , nS, nS) which contains two FFNs (, , nS) which share the initial layer. Both FFNs have different average coupling delays (ms and ms; ms) and thus different resonance frequencies (cf. panel a); for the remaining connections the average coupling delays is ms. Whereas a synchronous pulse extinguishes after a few layers in the absence of oscillations (ms), it may propagate along the layers of one FFN or the other depending on the stimulation frequency (ms and ms; , nS, nS, ms). Panel (c) is a close-up view of the raster plot shown in (b).
Mentions: We illustrate this dependency in Fig. 8a indicating the resonance peaks for different . Here, the coupling delays between neurons of successive layers are drawn uniformly from an interval of length centered at , (7)

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