Reversed somatodendritic I_h gradient in a class of rat hippocampal neurons with pyramidal morphology

Abstract

In CA1 and neocortical pyramidal neurons, I h is present primarily in the dendrites. We asked if all neurons of a pyramidal morphology have a similar density of I h . We characterized a novel class of hippocampal neurons with pyramidal morphology found in the stratum radiatum, which we termed the 'pyramidal-like principal' (PLP) neuron. Morphological similarities to pyramidal neurons were verified by filling the neurons with biocytin. PLPs did not stain for markers associated with interneurons, and projected to both the septum and olfactory bulb. By using cell-attached patch-clamp recordings, we found that these neurons expressed a high density of I h in the soma that declined to a lower density in the dendrites, a pattern that is reversed compared to pyramidal neurons. The voltage-dependent activation and activation time constants of I h in the PLPs were similar to pyramidal neurons. Whole-cell patch-clamp recordings from the soma and dendrites of PLP neurons showed no significant differences in input resistance and local temporal summation between the two locations. Blockade of I h by ZD7288 increased the input resistance and temporal summation of simulated EPSPs, as in pyramidal neurons. When NMDA receptors were blocked, temporal summation at the soma of distal synaptic potentials was similar to that seen with current injections at the soma, suggesting a 'normalization' of temporal summation similar to that observed in pyramidal neurons. Thus, we have characterized a principal neuronal subtype in the hippocampus with a similar morphology but reversed I h somatodendritic gradient to that previously observed in CA1 hippocampal and neocortical pyramidal neurons.

Local and Global Effects ofIhDistribution in Dendrites of Mammalian Neurons

“…This challenges the commonly held view that the dendritic gradient of I h in pyramidal cells and normalization of temporal summation are causally related. Our findings are further supported by recent experiments showing that one can achieve normalization of summation even with a reverse somatodendritic gradient of I h (Bullis et al, 2007).…”

“…Interestingly, recent experiments on pyramidal-like principal neurons in the stratum radiatum region of hippocampus have revealed a reverse I h gradient with higher somatic than dendritic expression (Bullis et al, 2007).…”

Location matters: somatic and dendritic SK channels answer to distinct calcium signals

“…At rest, I h is a hyperpolarization-activated inward current that could depolarize distal dendrites of pyramidal cells (Biel et al 2009). Consistent with this notion, I h increases with distance from the soma in apical dendrites of layer V pyramidal neurons (Berger et al 2001; Stuart and Spruston 1998) as well as CA1 pyramidal neurons (Bullis et al 2007). Whereas SK channels are voltage independent and inhibition of I h has little effect on bAPs in basal dendrites (Acker and Antic 2009), I h could promote activation of distal low-threshold R-type channels by depolarizing the dendritic resting potential closer to activation threshold, even during strong attenuation of bAP amplitude, resulting in more efficient activation of SK channels.…”

Differential expression of HCN subunits alters voltage-dependent gating of h-channels in CA1 pyramidal neurons from dorsal and ventral hippocampus

“…The VHC-type gradient can be considered an augmented h-conductance gradient, as the underlying gradient of h-conductance density is functionally augmented by the distance-dependent depolarization of the V 1/2 of voltage-dependent h-channel gating (e.g., more h-conductance is present within the neuron's range of subthreshold membrane potentials because of the depolarizing shift in V 1/2 ). Although distance-dependent changes in the V 1/2 of I h have been described previously (Angelo et al 2007;Berger et al 2001;Bullis et al 2007; Kole et al 2006;Magee 1998), this aspect of the h-conductance gradient has received relatively little attention with regard to the integrative properties of dendrites. Future experiments will be directed toward understanding the respective roles that DHC-type and VHCtype h-conductance gradients play in dendritic integration for CA1 pyramidal neurons.…”