Active Action Potential Propagation but Not Initiation in Thalamic Interneuron Dendrites

Inhibitory interneurons of the dorsal lateral geniculate nucleus of the thalamus modulate the activity of thalamocortical cells in response to excitatory input through the release of inhibitory neurotransmitter from both axons and dendrites. The exact mechanisms by which release can occur from dendrites are, however, not well understood. Recent experiments using calcium imaging have suggested that Na/K-based action potentials can evoke calcium transients in dendrites via local active conductances, making the backpropagating action potential a candidate for dendritic neurotransmitter release. In this study, we used high temporal and spatial resolution voltage-sensitive dye imaging to assess the characteristics of dendritic voltage deflections in response to Na/K action potentials in interneurons of the mouse dorsal lateral geniculate nucleus. We found that trains or single action potentials elicited by somatic current injection or local synaptic stimulation rapidly and actively backpropagated throughout the entire dendritic arbor and into the fine filiform dendritic appendages known to release GABAergic vesicles. Action potentials always appeared first in the soma or proximal dendrite in response to somatic current injection or local synaptic stimulation, and the rapid backpropagation into the dendritic arbor depended upon voltage-gated sodium and tetraethylammonium chloride-sensitive potassium channels. Our results indicate that thalamic interneuron dendrites integrate synaptic inputs that initiate action potentials, most likely in the axon initial segment, that then backpropagate with high fidelity into the dendrites, resulting in a nearly synchronous release of GABA from both axonal and dendritic compartments.