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The Journal of Neuroscience, August 16, 2006, 26(33):8633-8645; doi:10.1523/JNEUROSCI.2333-06.2006

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Behavioral/Systems/Cognitive
Distinct Electrical and Chemical Connectivity Maps in the Thalamic Reticular Nucleus: Potential Roles in Synchronization and Sensation

Charlotte Deleuze and John R. Huguenard

Department of Neurology and Neurological Sciences, Stanford University School of Medicine, Stanford, California 94305

Correspondence should be addressed to John R. Huguenard, Neurology and Neurological Sciences, Stanford University School of Medicine, Room M016, Stanford, CA 94305-5122. Email: john.huguenard{at}stanford.edu

GABAergic neurons of the thalamic reticular nucleus (nRt) provide thalamocortical relay neurons with feedback inhibition that influences sensory processing and thalamocortical rhythm generation. Mutual interactions between reticular neurons coordinate oscillatory activities developed within the network during normal sleep and in absence epilepsy, but the chemical versus electrical nature of these connections and their functional influence remain controversial. Here, we investigated the incidence and spatial extent of intra-nRt connectivity in vitro in horizontal and coronal thalamic slices from rat. Laser scanning photostimulation activated presynaptic nRt cells during patch-clamp recordings of postsynaptic neurons. Photolysis of caged glutamate evoked GABAergic IPSCs and/or depolarizing events (spikelets, mediated via electrical coupling) in a large proportion of neurons, thus indicating connectivity with presynaptic cell(s). Synaptic inputs were organized along the major axis of the nucleus in the same orientation as, but commonly exceeding the extent of, dendritic arborization of the postsynaptic neuron. In the anteroposterior (horizontal) plane, chemical connectivity had higher incidence (60% of recorded neurons vs 40% in vertical plane) and longer spatial extent, whereas in the dorsoventral (vertical) plane, electrical coupling dominated (47% incidence vs 37% in horizontal plane) and was more widely distributed. These data demonstrate that both electrical and chemical synapses are prominent within nRt and suggest different roles for the two types of connections. We thus propose that, along the vertical plane, electrical connectivity will promote coordinated rhythmic activity of sleep and/or thalamocortical epilepsy, whereas along the horizontal plane, chemical connectivity will oppose widespread thalamocortical synchronization and modulate sensory throughput.

Key words: thalamus; synaptic transmission; caged compound; electrophysiology; oscillations; neural networks

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Received June 1, 2006; revised July 12, 2006; accepted July 13, 2006.

Correspondence should be addressed to John R. Huguenard, Neurology and Neurological Sciences, Stanford University School of Medicine, Room M016, Stanford, CA 94305-5122. Email: john.huguenard{at}stanford.edu

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