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The Journal of Neuroscience, October 15, 2002, 22(20):8992-9004

Postnatal Development of the Hyperpolarization-Activated Excitatory Current I_h in Mouse Hippocampal Pyramidal Neurons

Dmitry V. Vasilyev and Michael E. Barish

Division of Neurosciences, Beckman Research Institute of the City of Hope, Duarte, California 91010

The hyperpolarization-activated excitatory current I_h shapes rhythmic firing and other components of excitability in differentiating neurons, and may thus influence activity-dependent CNS development. We therefore studied developmental changes in I_h and underlying hyperpolarization-activated cyclic nucleotide-gated (HCN) channel subunits in pyramidal neurons of neonatal mouse hippocampus using electrophysiological and immunofluorescence approaches. I_h conductance (at 80 mV) tripled in CA3 neurons and quintupled in CA1 neurons between postnatal day 1 (P1) and P20; parallel changes in membrane area resulted in current density maxima at P5 in CA3 and P10 in CA1. Concurrently, I_h activation times fell sevenfold in CA3 and 10-fold in CA1. A computational model indicates that a decrease in I_h activation time will increase the rhythmic firing rate. Two mechanisms contributed to more rapid I_h activation at P20 in CA3 and CA1 neurons: a fall in the intrinsic time constants of two kinetic components, _fast and _slow, to 35-40% (at 90 mV) of their P1 values, and a preferential increase in fast component amplitude and contribution to I_h (from ~35% to ~74% of total). HCN1, HCN2, and HCN4 immunoreactivities showed independent temporal and spatial developmental patterns. HCN1 immunoreactivity was low at P1 and P5 and increased by P20. HCN2 immunoreactivity was detected at P1 and increased steadily up to P20. HCN4 immunoreactivity was initially low and showed a small increase by P20. We suggest that developmental increases in I_h amplitude and activation rate reflect changes in the number and underlying structure of I_h channels, and that I_h maturation may shape rhythmic activity important for hippocampal circuit maturation.

Key words: I_h; hyperpolarization-activated current; HCN channels; hippocampus; pyramidal neurons; development; immunofluorescence; patch clamp; whole-cell recording

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Copyright © 2002 Society for Neuroscience  0270-6474/02/22208992-13$05.00/0

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