Gap Junctions Compensate for Sublinear Dendritic Integration in an Inhibitory Network
By K. Vervaeke, A. Lorincz, Z. Nusser, R. Silver. 2012
122 citations recorded by the source corpus.
Spreading the Excitation Inhibitory interneurons balance network excitation, control spike-time precision of principal neurons, and control synchrony within and across brain regions. Vervaeke et al. (p. 1624, published online 8 March) combined electrophysiology, immunohistology, and numerical simulation to investigate the properties of Golgi cells, the main inhibitory interneurons in the input layer of the cerebellar cortex. The dendrites of these neurons were truly passive and acted as linear cables. Gap junctions were distributed nonuniformly on the Golgi cell surface, with a higher density on distal dendrites. Thus, gap junction-mediated lateral excitation preferentially enhanced the distal inputs, enabling distal synapses to drive network activity more effectively. Synaptic charge spreads into the dendrites of neighboring interneurons via dendritic gap junctions. Electrically coupled inhibitory interneurons dynamically control network excitability, yet little is known about how chemical and electrical synapses regulate their activity. Using two-photon glutamate uncaging and dendritic patch-clamp recordings, we found that the dendrites of cerebellar Golgi interneurons acted as passive cables. They conferred distance-dependent sublinear synaptic integration and weakened distal excitatory inputs. Gap junctions were present at a higher density on distal dendrites and contributed substantially to membrane conductance. Depolarization of one Golgi cell increased firing in its neighbors, and inclusion of dendritic gap junctions in interneuron network models enabled distal excitatory synapses to drive network activity more effectively. Our results suggest that dendritic gap junctions counteract sublinear dendritic integration by enabling excitatory synaptic charge to spread into the dendrites of neighboring inhibitory interneurons.
Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience, Molecular Biology
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Citations in the corpus
- Re-evaluating circuit mechanisms underlying pattern separation (2019, neutral): “, 2016), which enables them to respond to excitatory input in a concerted (Vervaeke et al., 2012) or desynchronized manner (Vervaeke et al.”
- Granule Cell Ascending Axon Excitatory Synapses onto Golgi Cells Implement a Potent Feedback Circuit in the Cerebellar Granular Layer (2013, background): “The passive properties of the thin apical dendrites of GoCs have been shown to exert significant low-pass filtering on synaptic currents recorded at the soma (Kanichay and Silver, 2008; Vervaeke et al., 2012).”
- Functional Properties of Dendritic Gap Junctions in Cerebellar Golgi Cells (2016, unknown): “Since active conductances in the perisomatic region (Vervaeke et al., 2012) can introduce a voltage dependence to the CC (Dugué et al., 2009; Haas et al., 2011), we made recordings in the presence of a cocktail of antagonists and channel blockers, that rendered the cell membranes passive…”
- Fast-spiking, parvalbumin+ GABAergic interneurons: From cellular design to microcircuit function (2014, background): “Finally, gap junctions may boost the efficacy of distal inputs and increase the average action potential frequency after repetitive synaptic stimulation of distal synapses (35).”