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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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Transition from non-propagating to propagating regime.(a) The probability  that a single neuron in the ground state (receiving homogenous background inputs) spikes within 10 ms after stimulation by a synchronous input pulse of strength . For neurons with linear dendritic interactions (additive coupling; solid line) the spiking probability increases continuously with increasing input . For neurons with nonlinear dendritic interactions (non-additive coupling; dashed line), inputs larger than the dendritic threshold  elicit a dendritic spike and therefore the spiking probability jumps to a constant value, , for . The probabilities are estimated from averaging over  single trials per connection strength. (b,c) Maps (2), specifying the average number of synchronously spiking neurons  in one layer given that in the previous layer  neurons have spiked synchronously; derived from the single neuron response probability in (a) for an isolated FFN (here , ). Different colors indicate different strengths of feed-forward connections (nS); panel (b) shows the map for additive and panel (c) for non-additive coupling. For weak connection strength there is only one fixed point  corresponding to the extinction of a synchronous pulse. With increasing coupling strength two additional fixed points  and  emerge via a tangent bifurcation. This bifurcation marks the transition from a non-propagating to a propagating regime.
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pcbi-1003940-g002: Transition from non-propagating to propagating regime.(a) The probability that a single neuron in the ground state (receiving homogenous background inputs) spikes within 10 ms after stimulation by a synchronous input pulse of strength . For neurons with linear dendritic interactions (additive coupling; solid line) the spiking probability increases continuously with increasing input . For neurons with nonlinear dendritic interactions (non-additive coupling; dashed line), inputs larger than the dendritic threshold elicit a dendritic spike and therefore the spiking probability jumps to a constant value, , for . The probabilities are estimated from averaging over single trials per connection strength. (b,c) Maps (2), specifying the average number of synchronously spiking neurons in one layer given that in the previous layer neurons have spiked synchronously; derived from the single neuron response probability in (a) for an isolated FFN (here , ). Different colors indicate different strengths of feed-forward connections (nS); panel (b) shows the map for additive and panel (c) for non-additive coupling. For weak connection strength there is only one fixed point corresponding to the extinction of a synchronous pulse. With increasing coupling strength two additional fixed points and emerge via a tangent bifurcation. This bifurcation marks the transition from a non-propagating to a propagating regime.

Mentions: We assess the temporal development of the size of the synchronous pulse in every layer by considering the average number of neurons spiking synchronously in layer as a function of the average number synchronous spiking neurons in the preceding layer . Thus, replacing by and by in Equation (1) we obtain the map (2)where is the continuous interpolation of the right hand-side of Equation (1) for continuous . The fixed points of the map (2) determine the stability region for the propagation of synchrony (cf. Fig. 2). For small coupling strength , there is only one fixed point and any synchrony propagation will extinguish within few layers (cf. also Fig. 1b,e). For sufficiently large layer size and coupling strengths , stable propagation of synchrony can be achieved, the size and temporal spread of the synchronous pulse are stable throughout the layers (for an extensive analysis see [31]): This is due to the appearance of two additional fixed points, (unstable) and (stable), which emerge via a tangent bifurcation in the map (2) upon increasing . A synchronous pulse will propagate with a typical group size .


Oscillation-induced signal transmission and gating in neural circuits.

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

Transition from non-propagating to propagating regime.(a) The probability  that a single neuron in the ground state (receiving homogenous background inputs) spikes within 10 ms after stimulation by a synchronous input pulse of strength . For neurons with linear dendritic interactions (additive coupling; solid line) the spiking probability increases continuously with increasing input . For neurons with nonlinear dendritic interactions (non-additive coupling; dashed line), inputs larger than the dendritic threshold  elicit a dendritic spike and therefore the spiking probability jumps to a constant value, , for . The probabilities are estimated from averaging over  single trials per connection strength. (b,c) Maps (2), specifying the average number of synchronously spiking neurons  in one layer given that in the previous layer  neurons have spiked synchronously; derived from the single neuron response probability in (a) for an isolated FFN (here , ). Different colors indicate different strengths of feed-forward connections (nS); panel (b) shows the map for additive and panel (c) for non-additive coupling. For weak connection strength there is only one fixed point  corresponding to the extinction of a synchronous pulse. With increasing coupling strength two additional fixed points  and  emerge via a tangent bifurcation. This bifurcation marks the transition from a non-propagating to a propagating regime.
© Copyright Policy
Related In: Results  -  Collection

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

pcbi-1003940-g002: Transition from non-propagating to propagating regime.(a) The probability that a single neuron in the ground state (receiving homogenous background inputs) spikes within 10 ms after stimulation by a synchronous input pulse of strength . For neurons with linear dendritic interactions (additive coupling; solid line) the spiking probability increases continuously with increasing input . For neurons with nonlinear dendritic interactions (non-additive coupling; dashed line), inputs larger than the dendritic threshold elicit a dendritic spike and therefore the spiking probability jumps to a constant value, , for . The probabilities are estimated from averaging over single trials per connection strength. (b,c) Maps (2), specifying the average number of synchronously spiking neurons in one layer given that in the previous layer neurons have spiked synchronously; derived from the single neuron response probability in (a) for an isolated FFN (here , ). Different colors indicate different strengths of feed-forward connections (nS); panel (b) shows the map for additive and panel (c) for non-additive coupling. For weak connection strength there is only one fixed point corresponding to the extinction of a synchronous pulse. With increasing coupling strength two additional fixed points and emerge via a tangent bifurcation. This bifurcation marks the transition from a non-propagating to a propagating regime.
Mentions: We assess the temporal development of the size of the synchronous pulse in every layer by considering the average number of neurons spiking synchronously in layer as a function of the average number synchronous spiking neurons in the preceding layer . Thus, replacing by and by in Equation (1) we obtain the map (2)where is the continuous interpolation of the right hand-side of Equation (1) for continuous . The fixed points of the map (2) determine the stability region for the propagation of synchrony (cf. Fig. 2). For small coupling strength , there is only one fixed point and any synchrony propagation will extinguish within few layers (cf. also Fig. 1b,e). For sufficiently large layer size and coupling strengths , stable propagation of synchrony can be achieved, the size and temporal spread of the synchronous pulse are stable throughout the layers (for an extensive analysis see [31]): This is due to the appearance of two additional fixed points, (unstable) and (stable), which emerge via a tangent bifurcation in the map (2) upon increasing . A synchronous pulse will propagate with a typical group size .

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