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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.


Neural network topology. Structure of the network model. (A) The actual spatial location of neurons in their corresponding two-dimensional layers is shown. Mossy fibers (MFs) are shown in green, Golgi cells (GoCs) in red and granule cells (GCs) and parallel fibers (PFs) in blue. Only 1% of the GCs and PFs are displayed for better visualization. (B) Schematic diagram illustrating the connectivity between the layers. MFs (green) excite both GCs (blue) and GoCs (red). The axons of GCs form ascending fibers, which bifurcate in the PF fiber layer and spread in each direction of the x axis. These PFs excite the GoCs along the way. By contrast, GoCs inhibit the GCs in their vicinities. Two inhibitory circuits driven by the excitatory MF inputs emerge from this synaptic organization. One is a feedforward (FF) inhibitory circuit and the other is a feedback (FB) inhibitory circuit. The FF circuit works through the MF-GoC-GC pathway, whereas the FB circuit works through the MF-GC-PF-GoC-GC pathway. (C) Inset showing the neurotransmitters and synaptic receptors used by each modeled synaptic connection. The GoC model has α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors (AMPAR), which are activated by MF or PF glutamatergic (Glu) terminals. The GC model has AMPAR and N-methyl-D-aspartic acid receptors (NMDAR; activated by MF Glu terminals), and GABAa receptors (GABAaR) (activated by GABAergic terminals (GABA) coming from the nearby GoCs).
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Figure 1: Neural network topology. Structure of the network model. (A) The actual spatial location of neurons in their corresponding two-dimensional layers is shown. Mossy fibers (MFs) are shown in green, Golgi cells (GoCs) in red and granule cells (GCs) and parallel fibers (PFs) in blue. Only 1% of the GCs and PFs are displayed for better visualization. (B) Schematic diagram illustrating the connectivity between the layers. MFs (green) excite both GCs (blue) and GoCs (red). The axons of GCs form ascending fibers, which bifurcate in the PF fiber layer and spread in each direction of the x axis. These PFs excite the GoCs along the way. By contrast, GoCs inhibit the GCs in their vicinities. Two inhibitory circuits driven by the excitatory MF inputs emerge from this synaptic organization. One is a feedforward (FF) inhibitory circuit and the other is a feedback (FB) inhibitory circuit. The FF circuit works through the MF-GoC-GC pathway, whereas the FB circuit works through the MF-GC-PF-GoC-GC pathway. (C) Inset showing the neurotransmitters and synaptic receptors used by each modeled synaptic connection. The GoC model has α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors (AMPAR), which are activated by MF or PF glutamatergic (Glu) terminals. The GC model has AMPAR and N-methyl-D-aspartic acid receptors (NMDAR; activated by MF Glu terminals), and GABAa receptors (GABAaR) (activated by GABAergic terminals (GABA) coming from the nearby GoCs).

Mentions: The basic cerebellar cortex circuitry responsible for the generation of oscillations is driven by mossy fibers (MF) that excite both GCs [13,14] and Golgi cells (GoCs) [15-17]. The axons of the GCs form ascending fibers that bifurcate in both directions in the parallel fiber (PF) layer [18,19]. These PFs excite GoCs along their way. By contrast, GoCs are the only source of inhibition for the GCs in their vicinities [20]. Two inhibitory loops driven by the excitatory MF inputs emerge from this synaptic organization [21] (Figure 1B): a feedforward (FF) inhibitory loop and a feedback (FB) one. The FF loop works through the MF-GoC-GC pathway. MFs excite GoCs that then inhibit GCs. The FB loop works through the MF-GC-PF-GoC-GC pathway. MFs excite GCs that then excite GoCs that will inhibit GCs.


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

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

Neural network topology. Structure of the network model. (A) The actual spatial location of neurons in their corresponding two-dimensional layers is shown. Mossy fibers (MFs) are shown in green, Golgi cells (GoCs) in red and granule cells (GCs) and parallel fibers (PFs) in blue. Only 1% of the GCs and PFs are displayed for better visualization. (B) Schematic diagram illustrating the connectivity between the layers. MFs (green) excite both GCs (blue) and GoCs (red). The axons of GCs form ascending fibers, which bifurcate in the PF fiber layer and spread in each direction of the x axis. These PFs excite the GoCs along the way. By contrast, GoCs inhibit the GCs in their vicinities. Two inhibitory circuits driven by the excitatory MF inputs emerge from this synaptic organization. One is a feedforward (FF) inhibitory circuit and the other is a feedback (FB) inhibitory circuit. The FF circuit works through the MF-GoC-GC pathway, whereas the FB circuit works through the MF-GC-PF-GoC-GC pathway. (C) Inset showing the neurotransmitters and synaptic receptors used by each modeled synaptic connection. The GoC model has α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors (AMPAR), which are activated by MF or PF glutamatergic (Glu) terminals. The GC model has AMPAR and N-methyl-D-aspartic acid receptors (NMDAR; activated by MF Glu terminals), and GABAa receptors (GABAaR) (activated by GABAergic terminals (GABA) coming from the nearby GoCs).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Neural network topology. Structure of the network model. (A) The actual spatial location of neurons in their corresponding two-dimensional layers is shown. Mossy fibers (MFs) are shown in green, Golgi cells (GoCs) in red and granule cells (GCs) and parallel fibers (PFs) in blue. Only 1% of the GCs and PFs are displayed for better visualization. (B) Schematic diagram illustrating the connectivity between the layers. MFs (green) excite both GCs (blue) and GoCs (red). The axons of GCs form ascending fibers, which bifurcate in the PF fiber layer and spread in each direction of the x axis. These PFs excite the GoCs along the way. By contrast, GoCs inhibit the GCs in their vicinities. Two inhibitory circuits driven by the excitatory MF inputs emerge from this synaptic organization. One is a feedforward (FF) inhibitory circuit and the other is a feedback (FB) inhibitory circuit. The FF circuit works through the MF-GoC-GC pathway, whereas the FB circuit works through the MF-GC-PF-GoC-GC pathway. (C) Inset showing the neurotransmitters and synaptic receptors used by each modeled synaptic connection. The GoC model has α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors (AMPAR), which are activated by MF or PF glutamatergic (Glu) terminals. The GC model has AMPAR and N-methyl-D-aspartic acid receptors (NMDAR; activated by MF Glu terminals), and GABAa receptors (GABAaR) (activated by GABAergic terminals (GABA) coming from the nearby GoCs).
Mentions: The basic cerebellar cortex circuitry responsible for the generation of oscillations is driven by mossy fibers (MF) that excite both GCs [13,14] and Golgi cells (GoCs) [15-17]. The axons of the GCs form ascending fibers that bifurcate in both directions in the parallel fiber (PF) layer [18,19]. These PFs excite GoCs along their way. By contrast, GoCs are the only source of inhibition for the GCs in their vicinities [20]. Two inhibitory loops driven by the excitatory MF inputs emerge from this synaptic organization [21] (Figure 1B): a feedforward (FF) inhibitory loop and a feedback (FB) one. The FF loop works through the MF-GoC-GC pathway. MFs excite GoCs that then inhibit GCs. The FB loop works through the MF-GC-PF-GoC-GC pathway. MFs excite GCs that then excite GoCs that will inhibit GCs.

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.