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

Abstract

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.

A gain in GABA A receptor synaptic strength in thalamus reduces oscillatory activity and absence seizures

“…Anatomically, nRT neurons project collaterals onto adjacent nRT neurons that form axo-dendritic and dendro-dendritic synapses, which interconnect a powerful inhibitory network of cells that control the output of the dorsal thalamus to the cortex (26,27). Previous studies have provided the initial evidence that inhibitory intra-nRT synapses are integral in the oscillatory process.…”

Recurrent Circuits in Layer II of Medial Entorhinal Cortex in a Model of Temporal Lobe Epilepsy

“…Glutamate uncaging was performed as described previously (Deleuze and Huguenard, 2006;Jin el. al., 2006).…”

“…We evaluated several parameters to quantify characteristics of synaptic connectivity (Deleuze and Huguenard, 2006;Jin et al, 2006). Photostimulation sites were identified as responding if at least one postsynaptic current was detected within the measurement window.…”

Regulation of Inhibitory Synapses by Presynaptic D4 Dopamine Receptors in Thalamus

“…We next tested if DA could modulate intra-TRN inhibition considering these neurons form chemical synapses with each other (Deleuze and Huguenard 2006;Lam et al 2006;Shu and McCormick 2002). To evoke intra-TRN inhibitory responses, we focally applied glutamate via pressure ejection within TRN near our recording.…”

“…In addition, TRN receives GABAergic projections from globus pallidus (GP), substantia nigra pars reticulata (SNr), and basal forebrain (Anaya-Martinez et al 2006;Asanuma and Porter 1990;Asanuma 1994;Bickford et al 1994;Gandia et al 1993;Hazrati and Parent 1991;Pare et al 1990). Inhibitory innervations within TRN arise from local collaterals (Deleuze and Huguenard 2006;Lam et al 2006;Shu and McCormick 2002). GABAergic terminals within TRN are hypothesized to express D 4 receptors (Ariano et al 1997;Defagot et al 1997;Mrzljak et al 1996); however, the action of DA on GABAergic inhibitory signaling in TRN has not been explored.…”