Desynchronization of an electrically coupled interneuron network with excitatory synaptic input
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1
University College London, United Kingdom
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2
Institute of Experimental Medicine, Hungary
It is well established that the electrical synapses made between interneurons contribute to their synchronized firing behaviour and to the generation of network oscillations in a number of brain regions. However, relatively little is known about how coupled interneuron networks respond to excitatory synaptic inputs that occur during a sensory stimulus. To address this we studied a network of electrically coupled interneurons in the input layer of the cerebellar cortex. This network is particularly suited to this type of investigation because inhibitory Golgi cells only form chemical synapses with granule cells and not with one another, allowing electrical signalling to be studied in isolation. Using paired whole-cell recordings and synaptic stimulation in acute slices, we show that a sparse, temporally precise, excitatory mossy fibre input triggers a spike followed by a pause, in directly innervated Golgi cells, while a pause-only response was observed in the spontaneous firing of cells that do not receive direct excitatory synaptic inputs. Moreover, mossy fibre input also caused transient desynchonization of firing in the cell pair. Our results show that inhibition of neighbouring cells and desynchonization is caused by propagation of the action potential after-hyperpolarization through gap junctions. Biologically detailed computer simulations of Golgi cells using reconstructed cell morphologies, active conductances, measured gap junction locations and strengths, together with synaptic input distributed on the dendritic tree closely reproduced the results obtained with paired recordings. To explore the spatial properties of network dynamics we extended our two-cell model to a larger 3D network that incorporated the spatial dependence of connection probability and coupling coefficient measured from paired recordings, using the software application NeuroConstruct. The 3D network model consisted of 45 Golgi cells. Simulations run on parallel NEURON predict that rhythmically active Golgi cells synchronized in the absence of correlated synaptic inputs. However, sparse synaptic excitation of the Golgi cell network caused a transient desynchronization of spiking, with cells exhibiting a mosaic of excitation-pause and pause only responses. Our results suggest that several features of the sensory-evoked behaviour of Golgi cells and the rapid disappearance of granule cell oscillations observed in vivo could arise from sparse excitation of the electrically coupled Golgi cell network. Funded by BBSRC, MRC, EUSynapse and the Wellcome Trust.
Conference:
Computational and Systems Neuroscience 2010, Salt Lake City, UT, United States, 25 Feb - 2 Mar, 2010.
Presentation Type:
Oral Presentation
Topic:
Oral presentations
Citation:
Vervaeke
K,
Lorincz
A,
Gleeson
P,
Farinella
M,
Nusser
Z and
Silver
RA
(2010). Desynchronization of an electrically coupled interneuron network with excitatory synaptic input.
Front. Neurosci.
Conference Abstract:
Computational and Systems Neuroscience 2010.
doi: 10.3389/conf.fnins.2010.03.00005
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Received:
17 Feb 2010;
Published Online:
17 Feb 2010.
*
Correspondence:
R. A Silver, University College London, London, United Kingdom, a.silver@ucl.ac.uk