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

By Koen Vervaeke, A. Lorincz, Padraig Gleeson, Matteo Farinella, Zoltan Nusser, R. A. Silver. 2010

116 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): “…control (Eccles et al., 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…”
• Structured Connectivity in Cerebellar Inhibitory Networks (2014, unknown): “The level of synchrony of IPSCs has been used previously as a measure for the likelihood of two neurons sharing a presynaptic partner (Sippy and Yuste, 2013; Vincent and Marty, 1993).”
• Identification of an inhibitory circuit that regulates cerebellar Golgi cell activity (2012, unknown): “…studies have shown that Golgi cells are the only inhibitory cell in the cerebellar cortex to express mGluR2 and that the selective group II mGluR agonist (2R,4R)-APDC strongly hyperpolarizes Golgi cells to silence their spontaneous spiking (Ohishi et al., 1994; Watanabe and Nakanishi, 2003).”
• Functional Properties of Dendritic Gap Junctions in Cerebellar Golgi Cells (2016, unknown): “…two-photon or confocal guided patch-clamp recordings from dendrites (Nevian et al., 2007) have allowed direct electrical access to thin IN dendrites, including those of basket cells of the hippocampus (Hu et al., 2010; Nörenberg et al., 2010) and GoCs of the cerebellum (Vervaeke et al., 2012).”
• A novel inhibitory nucleo-cortical circuit controls cerebellar Golgi cell activity (2015, unknown): “Such an arrangement could partly explain the synchronization of Golgi cell activity observed along the axis of the lobules (Vos et al., 1999).”
• Inhibitory synaptic plasticity: spike timing-dependence and putative network function (2013, unknown): “…processing, synaptic plasticity, and prevention of epilepsy (Van Vreeswijk and Sompolinsky, 1996; Moore and Nelson, 1998; Wehr and Zador, 2003; Vogels and Abbott, 2005; Higley and Contreras, 2006; Froemke et al., 2007; de la Rocha et al., 2008; Monier et al., 2008; Okun and Lampl, 2008;…”
• Pathway-Specific Drive of Cerebellar Golgi Cells Reveals Integrative Rules of Cortical Inhibition (2018, unknown): “GoC basal dendrites were distinguishable from axons by their larger diameter (0.3 - 3.2 μm) and smooth surface devoid of boutons as previous described (Palay and Chan-Palay, 1974; Hull and Regehr, 2012; Vervaeke et al., 2012; Ankri et al., 2015; Rudolph et al., 2015; Szoboszlay et al., 2016).”