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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.


Electrical coupling between two Golgi cells (GoCs) connected by gap junctions either on the soma (red) or on the dendrite (black). Membrane potentials recorded from the soma of two gap junction-coupled GoCs in response to either (A, B) mossy fiber (MF) synaptic input at 10 Hz or (C, D) to a depolarizing current pulse. GoC1 and GoC2 were coupled by gap junctions either on the soma (red) or in the dendrite (black). (A, C) On the top, GoC1 is spiking and transmits to (B, D) thenon-spiking GoC2 below. In (C), pacemaker firing in GoC1 was suppressed with a hyperpolarizing current of -0.1 nA and a spike was evoked by a 100 ms pulse of 0.5 nA at 1500 ms. The spikes of GoC2 were always suppressed by setting all the sodium channel conductances to zero. Note (B, D) that the fast components of the spike (rising phase, peak and falling phase) are filtered more than the slower ones (undershoot), and that gap junction location does not matter much (red and black curves are superimposed). Dotted lines indicate the GoC resting membrane potential.
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Figure 3: Electrical coupling between two Golgi cells (GoCs) connected by gap junctions either on the soma (red) or on the dendrite (black). Membrane potentials recorded from the soma of two gap junction-coupled GoCs in response to either (A, B) mossy fiber (MF) synaptic input at 10 Hz or (C, D) to a depolarizing current pulse. GoC1 and GoC2 were coupled by gap junctions either on the soma (red) or in the dendrite (black). (A, C) On the top, GoC1 is spiking and transmits to (B, D) thenon-spiking GoC2 below. In (C), pacemaker firing in GoC1 was suppressed with a hyperpolarizing current of -0.1 nA and a spike was evoked by a 100 ms pulse of 0.5 nA at 1500 ms. The spikes of GoC2 were always suppressed by setting all the sodium channel conductances to zero. Note (B, D) that the fast components of the spike (rising phase, peak and falling phase) are filtered more than the slower ones (undershoot), and that gap junction location does not matter much (red and black curves are superimposed). Dotted lines indicate the GoC resting membrane potential.

Mentions: The membrane potential response of a non-spiking GoC coupled by gap junctions to a spiking GoC is composed of a depolarizing component related to the rising and falling phases of the action potential, and a hyperpolarizing component linked to the undershoot phase [28]. This coupling effect of gap junctions is illustrated by two coupled GoC models showing one spiking GoC stimulated either by MF input (Figure 3A) or by a current pulse (Figure 3C), and transmitting the depolarizing and hyperpolarizing components of spikes to another GoC (Figure 3B, D), replicating experimental observations. Note that gap junctions placed between dendrites (Figure 3, black lines) or between somata (Figure 3, red lines) produced the same effect in our GoC models.


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

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

Electrical coupling between two Golgi cells (GoCs) connected by gap junctions either on the soma (red) or on the dendrite (black). Membrane potentials recorded from the soma of two gap junction-coupled GoCs in response to either (A, B) mossy fiber (MF) synaptic input at 10 Hz or (C, D) to a depolarizing current pulse. GoC1 and GoC2 were coupled by gap junctions either on the soma (red) or in the dendrite (black). (A, C) On the top, GoC1 is spiking and transmits to (B, D) thenon-spiking GoC2 below. In (C), pacemaker firing in GoC1 was suppressed with a hyperpolarizing current of -0.1 nA and a spike was evoked by a 100 ms pulse of 0.5 nA at 1500 ms. The spikes of GoC2 were always suppressed by setting all the sodium channel conductances to zero. Note (B, D) that the fast components of the spike (rising phase, peak and falling phase) are filtered more than the slower ones (undershoot), and that gap junction location does not matter much (red and black curves are superimposed). Dotted lines indicate the GoC resting membrane potential.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Electrical coupling between two Golgi cells (GoCs) connected by gap junctions either on the soma (red) or on the dendrite (black). Membrane potentials recorded from the soma of two gap junction-coupled GoCs in response to either (A, B) mossy fiber (MF) synaptic input at 10 Hz or (C, D) to a depolarizing current pulse. GoC1 and GoC2 were coupled by gap junctions either on the soma (red) or in the dendrite (black). (A, C) On the top, GoC1 is spiking and transmits to (B, D) thenon-spiking GoC2 below. In (C), pacemaker firing in GoC1 was suppressed with a hyperpolarizing current of -0.1 nA and a spike was evoked by a 100 ms pulse of 0.5 nA at 1500 ms. The spikes of GoC2 were always suppressed by setting all the sodium channel conductances to zero. Note (B, D) that the fast components of the spike (rising phase, peak and falling phase) are filtered more than the slower ones (undershoot), and that gap junction location does not matter much (red and black curves are superimposed). Dotted lines indicate the GoC resting membrane potential.
Mentions: The membrane potential response of a non-spiking GoC coupled by gap junctions to a spiking GoC is composed of a depolarizing component related to the rising and falling phases of the action potential, and a hyperpolarizing component linked to the undershoot phase [28]. This coupling effect of gap junctions is illustrated by two coupled GoC models showing one spiking GoC stimulated either by MF input (Figure 3A) or by a current pulse (Figure 3C), and transmitting the depolarizing and hyperpolarizing components of spikes to another GoC (Figure 3B, D), replicating experimental observations. Note that gap junctions placed between dendrites (Figure 3, black lines) or between somata (Figure 3, red lines) produced the same effect in our GoC models.

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.