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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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Propagation frequency of a synchronous pulse.(a) Spike latency  of a neuron after stimulation with an input of strength  (shaded areas indicate the regions between the 0.2 and 0.8 quantiles; only data for  are shown). For neurons with nonlinear dendritic interactions  is constant, whereas for neurons with linear dendritic interactions  decreases with increasing stimulation strength . (b) Propagation frequency  of a synchronous pulse versus strength of the feed-forward connections  in the absence of external oscillations (, ); the inset shows a zoomed view of the propagation frequency in FFNs with non-additive couplings for . The yellow line indicates the natural propagation frequency .
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pcbi-1003940-g003: Propagation frequency of a synchronous pulse.(a) Spike latency of a neuron after stimulation with an input of strength (shaded areas indicate the regions between the 0.2 and 0.8 quantiles; only data for are shown). For neurons with nonlinear dendritic interactions is constant, whereas for neurons with linear dendritic interactions decreases with increasing stimulation strength . (b) Propagation frequency of a synchronous pulse versus strength of the feed-forward connections in the absence of external oscillations (, ); the inset shows a zoomed view of the propagation frequency in FFNs with non-additive couplings for . The yellow line indicates the natural propagation frequency .

Mentions: For networks with linear dendrites, decreases with increasing input strength (cf. Fig. 3a): The increase of the input causes a steeper and steeper rise of the evoked postsynaptic potential, and therefore reduces the (average) time the neuron needs to reach the threshold . In contrast, is constant for networks with nonlinear dendritic interactions: The spiking of the neuron is triggered by the additional current pulse mimicking the dendritic spike. This current pulse (and with it the resulting depolarization) is independent of the actual input strength (see also Methods Section), and the rise of the postsynaptic potential is so steep that is practically constant for . We note that for large input the spike latency for neurons with nonlinear dendritic interaction is larger than for neurons without: The latency between dendritic stimulation and the onset of the somatic response to the dendritic spike can be estimated to ms [29],[50], and is therefore delayed compared to the onset of the somatic response to the linear (electrically) transmitted signal.


Oscillation-induced signal transmission and gating in neural circuits.

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

Propagation frequency of a synchronous pulse.(a) Spike latency  of a neuron after stimulation with an input of strength  (shaded areas indicate the regions between the 0.2 and 0.8 quantiles; only data for  are shown). For neurons with nonlinear dendritic interactions  is constant, whereas for neurons with linear dendritic interactions  decreases with increasing stimulation strength . (b) Propagation frequency  of a synchronous pulse versus strength of the feed-forward connections  in the absence of external oscillations (, ); the inset shows a zoomed view of the propagation frequency in FFNs with non-additive couplings for . The yellow line indicates the natural propagation frequency .
© Copyright Policy
Related In: Results  -  Collection

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

pcbi-1003940-g003: Propagation frequency of a synchronous pulse.(a) Spike latency of a neuron after stimulation with an input of strength (shaded areas indicate the regions between the 0.2 and 0.8 quantiles; only data for are shown). For neurons with nonlinear dendritic interactions is constant, whereas for neurons with linear dendritic interactions decreases with increasing stimulation strength . (b) Propagation frequency of a synchronous pulse versus strength of the feed-forward connections in the absence of external oscillations (, ); the inset shows a zoomed view of the propagation frequency in FFNs with non-additive couplings for . The yellow line indicates the natural propagation frequency .
Mentions: For networks with linear dendrites, decreases with increasing input strength (cf. Fig. 3a): The increase of the input causes a steeper and steeper rise of the evoked postsynaptic potential, and therefore reduces the (average) time the neuron needs to reach the threshold . In contrast, is constant for networks with nonlinear dendritic interactions: The spiking of the neuron is triggered by the additional current pulse mimicking the dendritic spike. This current pulse (and with it the resulting depolarization) is independent of the actual input strength (see also Methods Section), and the rise of the postsynaptic potential is so steep that is practically constant for . We note that for large input the spike latency for neurons with nonlinear dendritic interaction is larger than for neurons without: The latency between dendritic stimulation and the onset of the somatic response to the dendritic spike can be estimated to ms [29],[50], and is therefore delayed compared to the onset of the somatic response to the linear (electrically) transmitted signal.

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