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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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FFNs with nonlinear dendritic interactions show resonance.Same network setup as in Fig. 4; coupling strengths are (a) nS, (b) nS and (c,d) nS. (a–c) The upper panels display the propagation frequency  of the synchronous signal, the lower panels show the layer up to which propagation occurs, as a function of the stimulation frequency  for FFNs with (a,b) linear and (c) nonlinear dendritic interactions. Different colors represent different amplitudes  of external oscillations as indicated by insets. In additively coupled FFNs (a) balanced oscillations hinder synchrony propagation, whereas (b) unbalanced oscillations (, i.e., excitation exceeds inhibition, cf. Equation 4) support it. This support, however, might be equally well achieved by temporally constant additional excitatory inputs: The thick gray filled lines indicate the propagation properties of an FFN, where single neurons receive constant additional current  (red; upper vertical axis),  (black) or (blue). For very strong depolarization (high  or ) the network enters a pathological activity state; this break-down of network stability is indicated by the vertical lines in the lower panel. In non-additively coupled FFNs even (c) balanced oscillations foster synchrony propagation and, in contrast to additively coupled FFNs, the propagating signal may lock to the oscillatory stimulation if the ratio  is rational; the gray lines indicate . This locking is illustrated in (d): Raster plots of spikes of the external oscillating population (upper panel) and of the FFN (lower panel). The yellow lines indicate the time intervals  for , containing  of the spikes of the external oscillatory population (cf. also Fig. 7).
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pcbi-1003940-g006: FFNs with nonlinear dendritic interactions show resonance.Same network setup as in Fig. 4; coupling strengths are (a) nS, (b) nS and (c,d) nS. (a–c) The upper panels display the propagation frequency of the synchronous signal, the lower panels show the layer up to which propagation occurs, as a function of the stimulation frequency for FFNs with (a,b) linear and (c) nonlinear dendritic interactions. Different colors represent different amplitudes of external oscillations as indicated by insets. In additively coupled FFNs (a) balanced oscillations hinder synchrony propagation, whereas (b) unbalanced oscillations (, i.e., excitation exceeds inhibition, cf. Equation 4) support it. This support, however, might be equally well achieved by temporally constant additional excitatory inputs: The thick gray filled lines indicate the propagation properties of an FFN, where single neurons receive constant additional current (red; upper vertical axis), (black) or (blue). For very strong depolarization (high or ) the network enters a pathological activity state; this break-down of network stability is indicated by the vertical lines in the lower panel. In non-additively coupled FFNs even (c) balanced oscillations foster synchrony propagation and, in contrast to additively coupled FFNs, the propagating signal may lock to the oscillatory stimulation if the ratio is rational; the gray lines indicate . This locking is illustrated in (d): Raster plots of spikes of the external oscillating population (upper panel) and of the FFN (lower panel). The yellow lines indicate the time intervals for , containing of the spikes of the external oscillatory population (cf. also Fig. 7).

Mentions: The panels show up to which layer the propagating synchronous pulse (initiated in the first layer in-phase with the external oscillations) is detectable (color-coded) as a function of the coupling strength and the amplitude of the external network oscillations, measured by . Configurations, where the system enters a pathological activity state (i.e., ongoing spontaneous propagation of synchrony) are marked in gray. Panels (a,c) show simulation results for networks with linear dendritic interactions (Hz, ms) and (b,d) for networks with nonlinear dendritic interactions (Hz, ms); panels (c) and (d) are close up views of (a) and (b). The black stars indicate the values of and used in Fig. 6a,c. Whereas balanced oscillations hinder signal propagation in additively coupled networks (i.e., require compensation by stronger coupling), they can support it in non-additively coupled ones. Other parameters are , nS, nS.


Oscillation-induced signal transmission and gating in neural circuits.

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

FFNs with nonlinear dendritic interactions show resonance.Same network setup as in Fig. 4; coupling strengths are (a) nS, (b) nS and (c,d) nS. (a–c) The upper panels display the propagation frequency  of the synchronous signal, the lower panels show the layer up to which propagation occurs, as a function of the stimulation frequency  for FFNs with (a,b) linear and (c) nonlinear dendritic interactions. Different colors represent different amplitudes  of external oscillations as indicated by insets. In additively coupled FFNs (a) balanced oscillations hinder synchrony propagation, whereas (b) unbalanced oscillations (, i.e., excitation exceeds inhibition, cf. Equation 4) support it. This support, however, might be equally well achieved by temporally constant additional excitatory inputs: The thick gray filled lines indicate the propagation properties of an FFN, where single neurons receive constant additional current  (red; upper vertical axis),  (black) or (blue). For very strong depolarization (high  or ) the network enters a pathological activity state; this break-down of network stability is indicated by the vertical lines in the lower panel. In non-additively coupled FFNs even (c) balanced oscillations foster synchrony propagation and, in contrast to additively coupled FFNs, the propagating signal may lock to the oscillatory stimulation if the ratio  is rational; the gray lines indicate . This locking is illustrated in (d): Raster plots of spikes of the external oscillating population (upper panel) and of the FFN (lower panel). The yellow lines indicate the time intervals  for , containing  of the spikes of the external oscillatory population (cf. also Fig. 7).
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Related In: Results  -  Collection

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

pcbi-1003940-g006: FFNs with nonlinear dendritic interactions show resonance.Same network setup as in Fig. 4; coupling strengths are (a) nS, (b) nS and (c,d) nS. (a–c) The upper panels display the propagation frequency of the synchronous signal, the lower panels show the layer up to which propagation occurs, as a function of the stimulation frequency for FFNs with (a,b) linear and (c) nonlinear dendritic interactions. Different colors represent different amplitudes of external oscillations as indicated by insets. In additively coupled FFNs (a) balanced oscillations hinder synchrony propagation, whereas (b) unbalanced oscillations (, i.e., excitation exceeds inhibition, cf. Equation 4) support it. This support, however, might be equally well achieved by temporally constant additional excitatory inputs: The thick gray filled lines indicate the propagation properties of an FFN, where single neurons receive constant additional current (red; upper vertical axis), (black) or (blue). For very strong depolarization (high or ) the network enters a pathological activity state; this break-down of network stability is indicated by the vertical lines in the lower panel. In non-additively coupled FFNs even (c) balanced oscillations foster synchrony propagation and, in contrast to additively coupled FFNs, the propagating signal may lock to the oscillatory stimulation if the ratio is rational; the gray lines indicate . This locking is illustrated in (d): Raster plots of spikes of the external oscillating population (upper panel) and of the FFN (lower panel). The yellow lines indicate the time intervals for , containing of the spikes of the external oscillatory population (cf. also Fig. 7).
Mentions: The panels show up to which layer the propagating synchronous pulse (initiated in the first layer in-phase with the external oscillations) is detectable (color-coded) as a function of the coupling strength and the amplitude of the external network oscillations, measured by . Configurations, where the system enters a pathological activity state (i.e., ongoing spontaneous propagation of synchrony) are marked in gray. Panels (a,c) show simulation results for networks with linear dendritic interactions (Hz, ms) and (b,d) for networks with nonlinear dendritic interactions (Hz, ms); panels (c) and (d) are close up views of (a) and (b). The black stars indicate the values of and used in Fig. 6a,c. Whereas balanced oscillations hinder signal propagation in additively coupled networks (i.e., require compensation by stronger coupling), they can support it in non-additively coupled ones. Other parameters are , nS, nS.

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