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Transient potassium channels augment degeneracy in hippocampal active dendritic spectral tuning.

Rathour RK, Malik R, Narayanan R - Sci Rep (2016)

Bottom Line: Modeling studies have predicted a critical regulatory role for A-type potassium (KA) channels towards augmenting functional robustness of this map.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.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.

View Article: PubMed Central - PubMed

Affiliation: Cellular Neurophysiology Laboratory, Molecular Biophysics Unit, Indian Institute of Science, Bangalore, India.

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.

No MeSH data available.


Related in: MedlinePlus

Weak pairwise correlations between intra-neuron percentage changes in different measurements after blockade of KA channels.(a,b) Left, Scatter plot matrix depicting the correlation between percentage changes among various measurements (at −65 mV) obtained from electrophysiological experiments using BaCl2 (a) or 3,4-DAP (b) to block KA channels. Color-coded matrix depicting the Pearson (Center) and Spearman (Right) correlation coefficient values for the corresponding scatter plots shown in the left. Percentage changes were pooled across all locations (a: n = 18; b: n = 21).
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f8: Weak pairwise correlations between intra-neuron percentage changes in different measurements after blockade of KA channels.(a,b) Left, Scatter plot matrix depicting the correlation between percentage changes among various measurements (at −65 mV) obtained from electrophysiological experiments using BaCl2 (a) or 3,4-DAP (b) to block KA channels. Color-coded matrix depicting the Pearson (Center) and Spearman (Right) correlation coefficient values for the corresponding scatter plots shown in the left. Percentage changes were pooled across all locations (a: n = 18; b: n = 21).

Mentions: To test the postulate using electrophysiological data, we computed the correlation coefficients between percentage changes among various measurements in response to blocking KA channels, either using BaCl2 (Fig. 8a) or 3,4-DAP (Fig. 8b). We found that most pairwise correlation coefficients (both Pearson and Spearman) between percentage changes among various measurements were weak, with only a small percentage showing higher correlations (BaCl2; Fig. 8a and 3,4-DAP; Fig. 8b). As these correlations were computed from measurements obtained from the same soma/dendrite, these results cannot be attributed to the differential expression of KA channels. Instead, these results suggest that KA channels differentially contribute to different physiological measurements of a given neuron, and underscore the critical role of interactions among different ion channels in regulating individual physiological measurements.


Transient potassium channels augment degeneracy in hippocampal active dendritic spectral tuning.

Rathour RK, Malik R, Narayanan R - Sci Rep (2016)

Weak pairwise correlations between intra-neuron percentage changes in different measurements after blockade of KA channels.(a,b) Left, Scatter plot matrix depicting the correlation between percentage changes among various measurements (at −65 mV) obtained from electrophysiological experiments using BaCl2 (a) or 3,4-DAP (b) to block KA channels. Color-coded matrix depicting the Pearson (Center) and Spearman (Right) correlation coefficient values for the corresponding scatter plots shown in the left. Percentage changes were pooled across all locations (a: n = 18; b: n = 21).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4837398&req=5

f8: Weak pairwise correlations between intra-neuron percentage changes in different measurements after blockade of KA channels.(a,b) Left, Scatter plot matrix depicting the correlation between percentage changes among various measurements (at −65 mV) obtained from electrophysiological experiments using BaCl2 (a) or 3,4-DAP (b) to block KA channels. Color-coded matrix depicting the Pearson (Center) and Spearman (Right) correlation coefficient values for the corresponding scatter plots shown in the left. Percentage changes were pooled across all locations (a: n = 18; b: n = 21).
Mentions: To test the postulate using electrophysiological data, we computed the correlation coefficients between percentage changes among various measurements in response to blocking KA channels, either using BaCl2 (Fig. 8a) or 3,4-DAP (Fig. 8b). We found that most pairwise correlation coefficients (both Pearson and Spearman) between percentage changes among various measurements were weak, with only a small percentage showing higher correlations (BaCl2; Fig. 8a and 3,4-DAP; Fig. 8b). As these correlations were computed from measurements obtained from the same soma/dendrite, these results cannot be attributed to the differential expression of KA channels. Instead, these results suggest that KA channels differentially contribute to different physiological measurements of a given neuron, and underscore the critical role of interactions among different ion channels in regulating individual physiological measurements.

Bottom Line: Modeling studies have predicted a critical regulatory role for A-type potassium (KA) channels towards augmenting functional robustness of this map.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.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.

View Article: PubMed Central - PubMed

Affiliation: Cellular Neurophysiology Laboratory, Molecular Biophysics Unit, Indian Institute of Science, Bangalore, India.

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.

No MeSH data available.


Related in: MedlinePlus