Abstract
Hippocampal pyramidal neurons express an intraneuronal map of spectral tuning mediated by hyperpolarization-activated cyclic-nucleotide-gated nonspecific-cation channels. Modeling studies have predicted a critical regulatory role for A-type potassium (KA) channels towards augmenting functional robustness of this map. To test this, we performed patch-clamp recordings from soma and dendrites of rat hippocampal pyramidal neurons, and measured spectral tuning before and after blocking KA channels using two structurally distinct pharmacological agents. Consistent with computational predictions, we found that blocking KA channels resulted in a significant reduction in resonance frequency and significant increases in input resistance, impedance amplitude and action-potential firing frequency across the somato-apical trunk. Furthermore, across all measured locations, blocking KA channels enhanced temporal summation of postsynaptic potentials and critically altered the impedance phase profile, resulting in a significant reduction in total inductive phase. Finally, pair-wise correlations between intraneuronal percentage changes (after blocking KA channels) in different measurements were mostly weak, suggesting differential regulation of different physiological properties by KA channels. Our results unveil a pivotal role for fast transient channels in regulating theta-frequency spectral tuning and intrinsic phase response, and suggest that degeneracy with reference to several coexisting functional maps is mediated by cross-channel interactions across the active dendritic arbor.
Highlights
Such elimination of spectral tuning with HCN-channel blockade, modeling frameworks have demonstrated that specific ion channels expressed in hippocampal pyramidal neurons could contribute to degeneracy in the somatodendritic expression of theta-frequency spectral tuning[2,7]
We measured Rin, action potential firing frequency and temporal summation strength (Sα), before and after blocking KA channels (Fig. 1) using either 200 μM BaCl222 or 150 μM 3,4-DAP23 in separate experiments, from soma or dendrites of CA1 pyramidal neurons
The prime conclusion of this study is that the fast and transient KA channels play a critical role in regulating the theta-frequency spectral tuning map along the somatoapical trunk of hippocampal pyramidal neurons
Summary
Such elimination of spectral tuning with HCN-channel blockade, modeling frameworks have demonstrated that specific ion channels expressed in hippocampal pyramidal neurons could contribute to degeneracy in the somatodendritic expression of theta-frequency spectral tuning[2,7]. Employing somatic and dendritic recordings from rat hippocampal pyramidal neurons, we positively test the predictions engendered from computational frameworks and unveil novel roles for KA channels in regulating theta-frequency spectral tuning, intrinsic phase response and excitability measurements across the somatoapical trunk.
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