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Robustness effect of gap junctions between Golgi cells on cerebellar cortex oscillations.

Simões de Souza FM, De Schutter E - Neural Syst Circuits (2011)

Bottom Line: Conversely, when GoCs were synaptically connected in the granular layer, gap junctions increased the power of the oscillations, but the oscillations were primarily driven by the synaptic feedback loop between GoCs and GCs, and the gap junctions did not change oscillation frequency or the mean firing rate of either GoCs or GCs.Our modeling results suggest that gap junctions between GoCs increase the robustness of cerebellar cortex oscillations that are primarily driven by the feedback loop between GoCs and GCs.The robustness effect of gap junctions on synaptically driven oscillations observed in our model may be a general mechanism, also present in other regions of the brain.

View Article: PubMed Central - HTML - PubMed

Affiliation: Computational Neuroscience Unit, Okinawa Institute of Science and Technology, Okinawa 904-0411, Japan. erik@oist.jp.

ABSTRACT

Background: Previous one-dimensional network modeling of the cerebellar granular layer has been successfully linked with a range of cerebellar cortex oscillations observed in vivo. However, the recent discovery of gap junctions between Golgi cells (GoCs), which may cause oscillations by themselves, has raised the question of how gap-junction coupling affects GoC and granular-layer oscillations. To investigate this question, we developed a novel two-dimensional computational model of the GoC-granule cell (GC) circuit with and without gap junctions between GoCs.

Results: Isolated GoCs coupled by gap junctions had a strong tendency to generate spontaneous oscillations without affecting their mean firing frequencies in response to distributed mossy fiber input. Conversely, when GoCs were synaptically connected in the granular layer, gap junctions increased the power of the oscillations, but the oscillations were primarily driven by the synaptic feedback loop between GoCs and GCs, and the gap junctions did not change oscillation frequency or the mean firing rate of either GoCs or GCs.

Conclusion: Our modeling results suggest that gap junctions between GoCs increase the robustness of cerebellar cortex oscillations that are primarily driven by the feedback loop between GoCs and GCs. The robustness effect of gap junctions on synaptically driven oscillations observed in our model may be a general mechanism, also present in other regions of the brain.

No MeSH data available.


The influence of gap junctions between Golgi cells (GoCs) on the responses of the network in the feedback loop configuration, with mossy fiber (MF) input at 100 Hz. (A) Feedback loop configuration: network with strong PF inputs and 100% synaptic weight. (B) Raster plot (top panel) and population spike timing histogram (PSTH) (bottom panel) of the GoC layer with (red) and without (blue) gap junctions. Each dot in the raster plot is a spike. MF mean firing rate (MFR) inputs at 100 Hz were turned on at the instant of 1000 ms. (C) Same as (B) but for the GC layer.
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Figure 9: The influence of gap junctions between Golgi cells (GoCs) on the responses of the network in the feedback loop configuration, with mossy fiber (MF) input at 100 Hz. (A) Feedback loop configuration: network with strong PF inputs and 100% synaptic weight. (B) Raster plot (top panel) and population spike timing histogram (PSTH) (bottom panel) of the GoC layer with (red) and without (blue) gap junctions. Each dot in the raster plot is a spike. MF mean firing rate (MFR) inputs at 100 Hz were turned on at the instant of 1000 ms. (C) Same as (B) but for the GC layer.

Mentions: We next investigated the effect of gap junctions on network oscillations under different conditions of MF activation and PF-connection strengths. We previously showed that the granular layer oscillates when the PF input to GoCs is strong (feedback configuration) and it is activated by MF input; conversely, in the absence of PF input (feedforward configuration) or of MF activation, GoC firing is desynchronized [9]. The latter is no longer true in the presence of gap junctions between GoCs (Figure 6). In the feedforward configuration, gap junction-coupled GoCs had a strong tendency to generate spontaneous slow and poorly synchronized GoC oscillations (Figure 6B, 800 to 1000 ms). Activation of MF input improved synchronization, and slightly increased oscillation frequency. Whereas gap junctions have a pronounced effect in the feedforward configuration, their effect is more subtle in the feedback configuration of the network, which more closely approximates the in vivo behavior of the granular layer [66-68] (Figure 7, Figure 8, Figure 9, Figure 10).


Robustness effect of gap junctions between Golgi cells on cerebellar cortex oscillations.

Simões de Souza FM, De Schutter E - Neural Syst Circuits (2011)

The influence of gap junctions between Golgi cells (GoCs) on the responses of the network in the feedback loop configuration, with mossy fiber (MF) input at 100 Hz. (A) Feedback loop configuration: network with strong PF inputs and 100% synaptic weight. (B) Raster plot (top panel) and population spike timing histogram (PSTH) (bottom panel) of the GoC layer with (red) and without (blue) gap junctions. Each dot in the raster plot is a spike. MF mean firing rate (MFR) inputs at 100 Hz were turned on at the instant of 1000 ms. (C) Same as (B) but for the GC layer.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3278348&req=5

Figure 9: The influence of gap junctions between Golgi cells (GoCs) on the responses of the network in the feedback loop configuration, with mossy fiber (MF) input at 100 Hz. (A) Feedback loop configuration: network with strong PF inputs and 100% synaptic weight. (B) Raster plot (top panel) and population spike timing histogram (PSTH) (bottom panel) of the GoC layer with (red) and without (blue) gap junctions. Each dot in the raster plot is a spike. MF mean firing rate (MFR) inputs at 100 Hz were turned on at the instant of 1000 ms. (C) Same as (B) but for the GC layer.
Mentions: We next investigated the effect of gap junctions on network oscillations under different conditions of MF activation and PF-connection strengths. We previously showed that the granular layer oscillates when the PF input to GoCs is strong (feedback configuration) and it is activated by MF input; conversely, in the absence of PF input (feedforward configuration) or of MF activation, GoC firing is desynchronized [9]. The latter is no longer true in the presence of gap junctions between GoCs (Figure 6). In the feedforward configuration, gap junction-coupled GoCs had a strong tendency to generate spontaneous slow and poorly synchronized GoC oscillations (Figure 6B, 800 to 1000 ms). Activation of MF input improved synchronization, and slightly increased oscillation frequency. Whereas gap junctions have a pronounced effect in the feedforward configuration, their effect is more subtle in the feedback configuration of the network, which more closely approximates the in vivo behavior of the granular layer [66-68] (Figure 7, Figure 8, Figure 9, Figure 10).

Bottom Line: Conversely, when GoCs were synaptically connected in the granular layer, gap junctions increased the power of the oscillations, but the oscillations were primarily driven by the synaptic feedback loop between GoCs and GCs, and the gap junctions did not change oscillation frequency or the mean firing rate of either GoCs or GCs.Our modeling results suggest that gap junctions between GoCs increase the robustness of cerebellar cortex oscillations that are primarily driven by the feedback loop between GoCs and GCs.The robustness effect of gap junctions on synaptically driven oscillations observed in our model may be a general mechanism, also present in other regions of the brain.

View Article: PubMed Central - HTML - PubMed

Affiliation: Computational Neuroscience Unit, Okinawa Institute of Science and Technology, Okinawa 904-0411, Japan. erik@oist.jp.

ABSTRACT

Background: Previous one-dimensional network modeling of the cerebellar granular layer has been successfully linked with a range of cerebellar cortex oscillations observed in vivo. However, the recent discovery of gap junctions between Golgi cells (GoCs), which may cause oscillations by themselves, has raised the question of how gap-junction coupling affects GoC and granular-layer oscillations. To investigate this question, we developed a novel two-dimensional computational model of the GoC-granule cell (GC) circuit with and without gap junctions between GoCs.

Results: Isolated GoCs coupled by gap junctions had a strong tendency to generate spontaneous oscillations without affecting their mean firing frequencies in response to distributed mossy fiber input. Conversely, when GoCs were synaptically connected in the granular layer, gap junctions increased the power of the oscillations, but the oscillations were primarily driven by the synaptic feedback loop between GoCs and GCs, and the gap junctions did not change oscillation frequency or the mean firing rate of either GoCs or GCs.

Conclusion: Our modeling results suggest that gap junctions between GoCs increase the robustness of cerebellar cortex oscillations that are primarily driven by the feedback loop between GoCs and GCs. The robustness effect of gap junctions on synaptically driven oscillations observed in our model may be a general mechanism, also present in other regions of the brain.

No MeSH data available.