Dendritic Ih ensures high-fidelity dendritic spike responses of motion-sensitive neurons in rat superior colliculus.
Hyperpolarization-activated cyclic nucleotide-gated (HCN) channels that generate I(h) currents are widely distributed in the brain and have been shown to contribute to various neuronal functions. In the present study, we investigated the functions of I(h) in the motion-sensitive projection neurons [wide field vertical (WFV) cells] of the superior colliculus, a pivotal visual center for detection of and orientating to salient objects. Combination of whole cell recordings and immunohistochemical investigations suggested that HCN1 channels dominantly contribute to the I(h) in WFV cells among HCN isoforms expressed in the superficial superior colliculus and mainly located on their expansive dendritic trees. We found that blocking I(h) suppressed the initiation of short- and fixed-latency dendritic spike responses and led instead to long- and fluctuating-latency somatic spike responses to optic fiber stimulations. These results suggest that the dendritic I(h) facilitates the dendritic initiation and/or propagation of action potentials and ensures that WFV cells generate spike responses to distal synaptic inputs in a sensitive and robustly time-locked manner, probably by acting as continuous depolarizing drive and fixing dendritic membrane potentials close to the spike threshold. These functions are different from known functions of dendritic I(h) revealed in hippocampal and neocortical pyramidal cells, where they spatiotemporally limit the propagations of synaptic inputs along the apical dendrites by reducing dendritic membrane resistance. Thus we have revealed new functional aspects of I(h), and these dendritic properties are likely critical for visual motion processing in these neurons.
Endo
Toshiaki
T
Division of Behavioral Development, Department of Developmental Physiology, Center for Genetic Analysis of Behavior, National Institute for Physiological Sciences, Okazaki, Japan. toshiaki.endo@ki.se
Tarusawa
Etsuko
E
Notomi
Takuya
T
Kaneda
Katsuyuki
K
Hirabayashi
Masumi
M
Shigemoto
Ryuichi
R
Isa
Tadashi
T
D000200:Action Potentials / Q000502:physiology; D000818:Animals; D002316:Cardiotonic Agents / Q000494:pharmacology; D054815:Cyclic Nucleotide-Gated Cation Channels / Q000187:drug effects / Q000502:physiology*; D003627:Data Interpretation, Statistical; D003712:Dendrites / Q000187:drug effects / Q000502:physiology*; D004594:Electrophysiology; D019706:Excitatory Postsynaptic Potentials / Q000187:drug effects; D005336:Fiber Optic Technology; D064428:Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels; D007150:Immunohistochemistry; D017403:In Situ Hybridization; D008564:Membrane Potentials / Q000502:physiology; D009039:Motion Perception / Q000187:drug effects / Q000502:physiology*; D010775:Photic Stimulation; D015221:Potassium Channels / Q000187:drug effects / Q000502:physiology*; D011743:Pyrimidines / Q000494:pharmacology; D051381:Rats; D020318:Rats, Long-Evans; D017208:Rats, Wistar; D013477:Superior Colliculi / Q000166:cytology / Q000187:drug effects / Q000502:physiology*; D013569:Synapses / Q000187:drug effects / Q000502:physiology; D013570:Synaptic Membranes / Q000187:drug effects / Q000502:physiology
D002316:Cardiotonic Agents; D054815:Cyclic Nucleotide-Gated Cation Channels; C578667:Hcn1 protein, rat; D064428:Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels; D015221:Potassium Channels; D011743:Pyrimidines; C082246:ICI D2788