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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

Support of propagation of synchrony by unbalanced oscillations.Same setup as in Fig. 4, but with altered inhibitory coupling strength  as indicated in (b). The lines inclose the parameter regions for which an initial synchronous pulse is detectable up to the final layer. (a) For FFNs with linear dendritic interactions unbalanced oscillations may foster propagation of synchrony, if the excitation exceeds the inhibition (, i.e., ; red lines) or impede it, if the inhibition exceeds the excitation, respectively (, i.e., ; blue lines). (b) In contrast, in FFNs with nonlinear dendritic interactions the balance between excitation and inhibition has only a weak effect on the parameter region in which robust propagation of synchrony is possible.
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pcbi-1003940-g005: Support of propagation of synchrony by unbalanced oscillations.Same setup as in Fig. 4, but with altered inhibitory coupling strength as indicated in (b). The lines inclose the parameter regions for which an initial synchronous pulse is detectable up to the final layer. (a) For FFNs with linear dendritic interactions unbalanced oscillations may foster propagation of synchrony, if the excitation exceeds the inhibition (, i.e., ; red lines) or impede it, if the inhibition exceeds the excitation, respectively (, i.e., ; blue lines). (b) In contrast, in FFNs with nonlinear dendritic interactions the balance between excitation and inhibition has only a weak effect on the parameter region in which robust propagation of synchrony is possible.

Mentions: (4)For additively coupled networks and such input indeed promotes synchrony propagation (cf. Fig. 5a, red lines): The oscillatory input depolarizes the neurons of the FFN and thus less synaptic input is needed to elicit a somatic spike; the critical connectivity decreases. At the same time, the increased excitability of the neurons lowers the threshold for pathological activity, . Likewise, for the neurons are hyperpolarized by the oscillatory input which impedes the generation of somatic spikes; the critical connectivity increases (cf. Fig. 5a, blue lines).


Oscillation-induced signal transmission and gating in neural circuits.

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

Support of propagation of synchrony by unbalanced oscillations.Same setup as in Fig. 4, but with altered inhibitory coupling strength  as indicated in (b). The lines inclose the parameter regions for which an initial synchronous pulse is detectable up to the final layer. (a) For FFNs with linear dendritic interactions unbalanced oscillations may foster propagation of synchrony, if the excitation exceeds the inhibition (, i.e., ; red lines) or impede it, if the inhibition exceeds the excitation, respectively (, i.e., ; blue lines). (b) In contrast, in FFNs with nonlinear dendritic interactions the balance between excitation and inhibition has only a weak effect on the parameter region in which robust propagation of synchrony is possible.
© Copyright Policy
Related In: Results  -  Collection

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

pcbi-1003940-g005: Support of propagation of synchrony by unbalanced oscillations.Same setup as in Fig. 4, but with altered inhibitory coupling strength as indicated in (b). The lines inclose the parameter regions for which an initial synchronous pulse is detectable up to the final layer. (a) For FFNs with linear dendritic interactions unbalanced oscillations may foster propagation of synchrony, if the excitation exceeds the inhibition (, i.e., ; red lines) or impede it, if the inhibition exceeds the excitation, respectively (, i.e., ; blue lines). (b) In contrast, in FFNs with nonlinear dendritic interactions the balance between excitation and inhibition has only a weak effect on the parameter region in which robust propagation of synchrony is possible.
Mentions: (4)For additively coupled networks and such input indeed promotes synchrony propagation (cf. Fig. 5a, red lines): The oscillatory input depolarizes the neurons of the FFN and thus less synaptic input is needed to elicit a somatic spike; the critical connectivity decreases. At the same time, the increased excitability of the neurons lowers the threshold for pathological activity, . Likewise, for the neurons are hyperpolarized by the oscillatory input which impedes the generation of somatic spikes; the critical connectivity increases (cf. Fig. 5a, blue lines).

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