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Noise promotes independent control of gamma oscillations and grid firing within recurrent attractor networks.

Solanka L, van Rossum MC, Nolan MF - Elife (2015)

Bottom Line: Neural computations underlying cognitive functions require calibration of the strength of excitatory and inhibitory synaptic connections and are associated with modulation of gamma frequency oscillations in network activity.This beneficial role for noise results from disruption of epileptic-like network states.Our results have implications for tuning of normal circuit function and for disorders associated with changes in gamma oscillations and synaptic strength.

View Article: PubMed Central - PubMed

Affiliation: Centre for Integrative Physiology, University of Edinburgh, Edinburgh, United Kingdom.

ABSTRACT
Neural computations underlying cognitive functions require calibration of the strength of excitatory and inhibitory synaptic connections and are associated with modulation of gamma frequency oscillations in network activity. However, principles relating gamma oscillations, synaptic strength and circuit computations are unclear. We address this in attractor network models that account for grid firing and theta-nested gamma oscillations in the medial entorhinal cortex. We show that moderate intrinsic noise massively increases the range of synaptic strengths supporting gamma oscillations and grid computation. With moderate noise, variation in excitatory or inhibitory synaptic strength tunes the amplitude and frequency of gamma activity without disrupting grid firing. This beneficial role for noise results from disruption of epileptic-like network states. Thus, moderate noise promotes independent control of multiplexed firing rate- and gamma-based computational mechanisms. Our results have implications for tuning of normal circuit function and for disorders associated with changes in gamma oscillations and synaptic strength.

No MeSH data available.


Effect of noise on gridness scores in networks without theta frequency inputs.The plot shows a difference between gridness scores of networks with σ = 150 pA and networks with σ = 0 pA plotted as a function of gE and gI when theta inputs were replaced with a constant input with an equal mean amplitude.DOI:http://dx.doi.org/10.7554/eLife.06444.021
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fig6s2: Effect of noise on gridness scores in networks without theta frequency inputs.The plot shows a difference between gridness scores of networks with σ = 150 pA and networks with σ = 0 pA plotted as a function of gE and gI when theta inputs were replaced with a constant input with an equal mean amplitude.DOI:http://dx.doi.org/10.7554/eLife.06444.021

Mentions: Because seizure-like events tend to initiate early on the depolarizing phase of each theta cycle, we asked if synchronization by theta frequency drive plays a role in their initiation. When theta frequency input was replaced with a constant input with the same mean amplitude, the power of gamma oscillations was still dependent on the levels of noise and changes in gE and gI (Figure 6—figure supplement 1). However, in contrast to simulations with theta frequency input (Figure 5D,E), noise-free networks without theta exhibited hyper-synchronous firing only when gE was <0.5 nS (Figure 6A) and generated grid firing fields almost in the complete range of gE and gI (Figure 6D,G). Addition of noise in the absence of theta had mostly detrimental effects on grid firing (Figure 6E,F,H,I and Figure 6—figure supplement 2). Interestingly, with intermediate levels of noise, the subregion with high gridness scores (>0.5) retained its crescent-like shape (Figure 6E,H), but was smaller when compared to the networks with theta frequency inputs (size of regions with and without theta: 488/961 vs 438/961), while the range of gamma frequencies present was much lower than in networks containing theta drive. Together, these data indicate that moderate noise prevents emergence of seizure like states by disrupting synchronization of the attractor network by the shared theta frequency drive. In networks with moderate noise theta drive promotes grid firing and enables a wide range of gamma frequencies to be generated without disrupting grid firing.10.7554/eLife.06444.019Figure 6.Seizure-like states and grid firing fields in networks without theta frequency inputs.


Noise promotes independent control of gamma oscillations and grid firing within recurrent attractor networks.

Solanka L, van Rossum MC, Nolan MF - Elife (2015)

Effect of noise on gridness scores in networks without theta frequency inputs.The plot shows a difference between gridness scores of networks with σ = 150 pA and networks with σ = 0 pA plotted as a function of gE and gI when theta inputs were replaced with a constant input with an equal mean amplitude.DOI:http://dx.doi.org/10.7554/eLife.06444.021
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4508578&req=5

fig6s2: Effect of noise on gridness scores in networks without theta frequency inputs.The plot shows a difference between gridness scores of networks with σ = 150 pA and networks with σ = 0 pA plotted as a function of gE and gI when theta inputs were replaced with a constant input with an equal mean amplitude.DOI:http://dx.doi.org/10.7554/eLife.06444.021
Mentions: Because seizure-like events tend to initiate early on the depolarizing phase of each theta cycle, we asked if synchronization by theta frequency drive plays a role in their initiation. When theta frequency input was replaced with a constant input with the same mean amplitude, the power of gamma oscillations was still dependent on the levels of noise and changes in gE and gI (Figure 6—figure supplement 1). However, in contrast to simulations with theta frequency input (Figure 5D,E), noise-free networks without theta exhibited hyper-synchronous firing only when gE was <0.5 nS (Figure 6A) and generated grid firing fields almost in the complete range of gE and gI (Figure 6D,G). Addition of noise in the absence of theta had mostly detrimental effects on grid firing (Figure 6E,F,H,I and Figure 6—figure supplement 2). Interestingly, with intermediate levels of noise, the subregion with high gridness scores (>0.5) retained its crescent-like shape (Figure 6E,H), but was smaller when compared to the networks with theta frequency inputs (size of regions with and without theta: 488/961 vs 438/961), while the range of gamma frequencies present was much lower than in networks containing theta drive. Together, these data indicate that moderate noise prevents emergence of seizure like states by disrupting synchronization of the attractor network by the shared theta frequency drive. In networks with moderate noise theta drive promotes grid firing and enables a wide range of gamma frequencies to be generated without disrupting grid firing.10.7554/eLife.06444.019Figure 6.Seizure-like states and grid firing fields in networks without theta frequency inputs.

Bottom Line: Neural computations underlying cognitive functions require calibration of the strength of excitatory and inhibitory synaptic connections and are associated with modulation of gamma frequency oscillations in network activity.This beneficial role for noise results from disruption of epileptic-like network states.Our results have implications for tuning of normal circuit function and for disorders associated with changes in gamma oscillations and synaptic strength.

View Article: PubMed Central - PubMed

Affiliation: Centre for Integrative Physiology, University of Edinburgh, Edinburgh, United Kingdom.

ABSTRACT
Neural computations underlying cognitive functions require calibration of the strength of excitatory and inhibitory synaptic connections and are associated with modulation of gamma frequency oscillations in network activity. However, principles relating gamma oscillations, synaptic strength and circuit computations are unclear. We address this in attractor network models that account for grid firing and theta-nested gamma oscillations in the medial entorhinal cortex. We show that moderate intrinsic noise massively increases the range of synaptic strengths supporting gamma oscillations and grid computation. With moderate noise, variation in excitatory or inhibitory synaptic strength tunes the amplitude and frequency of gamma activity without disrupting grid firing. This beneficial role for noise results from disruption of epileptic-like network states. Thus, moderate noise promotes independent control of multiplexed firing rate- and gamma-based computational mechanisms. Our results have implications for tuning of normal circuit function and for disorders associated with changes in gamma oscillations and synaptic strength.

No MeSH data available.