Rapid Desynchronization of an Electrically Coupled Interneuron Network with Sparse Excitatory Synaptic Input

2010

176 citations recorded by the source corpus.

Summary Electrical synapses between interneurons contribute to synchronized firing and network oscillations in the brain. However, little is known about how such networks respond to excitatory synaptic input. To investigate this, we studied electrically coupled Golgi cells (GoC) in the cerebellar input layer. We show with immunohistochemistry, electron microscopy, and electrophysiology that Connexin-36 is necessary for functional gap junctions (GJs) between GoC dendrites. In the absence of coincident synaptic input, GoCs synchronize their firing. In contrast, sparse, coincident mossy fiber input triggered a mixture of excitation and inhibition of GoC firing and spike desynchronization. Inhibition is caused by propagation of the spike afterhyperpolarization through GJs. This triggers network desynchronization because heterogeneous coupling to surrounding cells causes spike-phase dispersion. Detailed network models predict that desynchronization is robust, local, and dependent on synaptic input properties. Our results show that GJ coupling can be inhibitory and either promote network synchronization or trigger rapid network desynchronization depending on the synaptic input.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience

Citations in the corpus

• Re-evaluating circuit mechanisms underlying pattern separation (2019, neutral): “…interconnected via chemical synapses (Hull and Regehr, 2012) and densely connected via electrical synapses (Dugue et al., 2009; Szoboszlay et al., 2016), which enables them to respond to excitatory input in a concerted (Vervaeke et al., 2012) or desynchronized manner (Vervaeke et al., 2010).”
• Granule Cell Ascending Axon Excitatory Synapses onto Golgi Cells Implement a Potent Feedback Circuit in the Cerebellar Granular Layer (2013, unknown): “, 1967; Marr, 1969; Albus, 1971), by creating oscillatory synchronization (Maex and De Schutter, 1998; Dugué et al., 2009; Vervaeke et al., 2010), by setting the time window for GrC excitation (D’Angelo and De Zeeuw, 2009), and by controlling long-term synaptic plasticity at mossy fiber (mf) synapse”
• Inhibitory synaptic plasticity: spike timing-dependence and putative network function (2013, unknown): “In many cases, inhibitory and electrical synapses play complementary roles in coordinating the activity of neurons and their inhibitory output, although electrical synapses have been shown to act as inhibitory de-synchronizers for some neurons (Vervaeke et al., 2010).”
• Structured Connectivity in Cerebellar Inhibitory Networks (2014, unknown): “%) followed by an afterhyperpolarization (AHP; 0.46 ± 0.58 mV, n = 77), as observed between other coupled cells with large AHPs (Galarreta andHestrin, 2002; Vervaeke et al., 2010; Figure S1).”
• A novel inhibitory nucleo-cortical circuit controls cerebellar Golgi cell activity (2015, unknown): “…some of the recorded Golgi cells, trains of light pulses elicited a time locking of intrinsic spikes (n = 7, Figure 3—figure supplement 1) without clear inhibitory effect, suggesting a network effect mediated through the gap junctions among Golgi cells (Dugué et al., 2009; Vervaeke et al., 2010).”
• Pathway-Specific Drive of Cerebellar Golgi Cells Reveals Integrative Rules of Cortical Inhibition (2018, unknown): “Another source of complexity in relating MF activity to recruitment of feedforward inhibition is the fact that EPSP-spike coupling in GoCs is heavily temporally filtered (Vervaeke et al., 2010; Kanichay and Silver, 2008).”
• Functional Properties of Dendritic Gap Junctions in Cerebellar Golgi Cells (2016, unknown): “However, prominent heterogeneity in coupling strength is also present among GoCs having similar intersomatic distances (Vervaeke et al., 2010).”