Action potential backpropagation and somato-dendritic distribution of ion channels in thalamocortical neurons

Abstract

Thalamocortical (TC) neurons of the dorsal thalamus integrate sensory inputs in an attentionally relevant manner during wakefulness and exhibit complex network-driven and intrinsic oscillatory activity during sleep. Despite these complex intrinsic and network functions, little is known about the dendritic distribution of ion channels in TC neurons or the role such channel distributions may play in synaptic integration. Here we demonstrate with simultaneous somatic and dendritic recordings from TC neurons in brain slices that action potentials evoked by sensory or cortical excitatory postsynaptic potentials are initiated near the soma and backpropagate into the dendrites of TC neurons. Cell-attached recordings demonstrated that TC neuron dendrites contain a nonuniform distribution of sodium but a roughly uniform density of potassium channels across the somatodendritic area examined that corresponds to approximately half the average path length of TC neuron dendrites. Dendritic action potential backpropagation was found to be active, but compromised by dendritic branching, such that action potentials may fail to invade relatively distal dendrites. We have also observed that calcium channels are nonuniformly distributed in the dendrites of TC neurons. Low-threshold calcium channels were found to be concentrated at proximal dendritic locations, sites known to receive excitatory synaptic connections from primary afferents, suggesting that they play a key role in the amplification of sensory inputs to TC neurons.