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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

Blocking KA channels resulted in a decrease in resonance frequency across the somatoapical trunk.(a) Same as Fig. 2a. (b) Voltage traces recorded from dendrites located at 240 μm (top) and 270 μm (bottom) away from soma in response to the Chirp15 stimulus under baseline condition (blue) and after blocking KA channels (orange), using BaCl2 (top) and 3,4-DAP (bottom), respectively. (c) Impedance amplitude plotted as functions of input current frequency derived from corresponding color-matched traces shown in (b), under baseline condition (blue) and after blocking KA channels (orange) using BaCl2 (top) or 3,4-DAP (bottom). (d,e) Population data (also depicted as quartiles) for the effect of blocking KA channels, using BaCl2 (d) or 3,4-DAP (e), on resonance frequency (fR) for the three sub-populations of recording locations. *p < 0.05 Mann Whitney U test. (f) Cumulative probability of percentage change in fR in response to blocking A-type K+ channels using BaCl2 (top) or 3,4-DAP (bottom). (g) Population data for percentage change in fR after blocking KA channels, using either BaCl2 (left) or 3,4-DAP (right), plotted as a function of recording location. Open circles represent individual cells and filled circles represent the average values (mean ± SEM).
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f4: Blocking KA channels resulted in a decrease in resonance frequency across the somatoapical trunk.(a) Same as Fig. 2a. (b) Voltage traces recorded from dendrites located at 240 μm (top) and 270 μm (bottom) away from soma in response to the Chirp15 stimulus under baseline condition (blue) and after blocking KA channels (orange), using BaCl2 (top) and 3,4-DAP (bottom), respectively. (c) Impedance amplitude plotted as functions of input current frequency derived from corresponding color-matched traces shown in (b), under baseline condition (blue) and after blocking KA channels (orange) using BaCl2 (top) or 3,4-DAP (bottom). (d,e) Population data (also depicted as quartiles) for the effect of blocking KA channels, using BaCl2 (d) or 3,4-DAP (e), on resonance frequency (fR) for the three sub-populations of recording locations. *p < 0.05 Mann Whitney U test. (f) Cumulative probability of percentage change in fR in response to blocking A-type K+ channels using BaCl2 (top) or 3,4-DAP (bottom). (g) Population data for percentage change in fR after blocking KA channels, using either BaCl2 (left) or 3,4-DAP (right), plotted as a function of recording location. Open circles represent individual cells and filled circles represent the average values (mean ± SEM).

Mentions: Computational models have predicted that KA channels, despite being fast transient channels, could alter low-frequency spectral tuning in CA1 pyramidal neuron somata and their dendrites27. To test this prediction, we measured the responses of soma or dendrites to a chirp current (0–15 Hz in 15 s; Fig. 1c) stimulus before and after blocking KA channels (Figs 1 and 4b). Quantifying frequency-dependent response properties of neurons from the voltage responses to the chirp stimulus (Fig. 4c), we found that blocking KA channels resulted in a decrease in resonance frequency, fR, across the somato-apical trunk (Fig. 4d,e) (Tables S1 and S2), with percentage changes not significantly different across the somato-apical trunk (Fig. 4f,g, BaCl2: p = 0.28 and 3,4-DAP: p = 0.43 Kruskal-Wallis rank sum test).


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

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

Blocking KA channels resulted in a decrease in resonance frequency across the somatoapical trunk.(a) Same as Fig. 2a. (b) Voltage traces recorded from dendrites located at 240 μm (top) and 270 μm (bottom) away from soma in response to the Chirp15 stimulus under baseline condition (blue) and after blocking KA channels (orange), using BaCl2 (top) and 3,4-DAP (bottom), respectively. (c) Impedance amplitude plotted as functions of input current frequency derived from corresponding color-matched traces shown in (b), under baseline condition (blue) and after blocking KA channels (orange) using BaCl2 (top) or 3,4-DAP (bottom). (d,e) Population data (also depicted as quartiles) for the effect of blocking KA channels, using BaCl2 (d) or 3,4-DAP (e), on resonance frequency (fR) for the three sub-populations of recording locations. *p < 0.05 Mann Whitney U test. (f) Cumulative probability of percentage change in fR in response to blocking A-type K+ channels using BaCl2 (top) or 3,4-DAP (bottom). (g) Population data for percentage change in fR after blocking KA channels, using either BaCl2 (left) or 3,4-DAP (right), plotted as a function of recording location. Open circles represent individual cells and filled circles represent the average values (mean ± SEM).
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Related In: Results  -  Collection

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f4: Blocking KA channels resulted in a decrease in resonance frequency across the somatoapical trunk.(a) Same as Fig. 2a. (b) Voltage traces recorded from dendrites located at 240 μm (top) and 270 μm (bottom) away from soma in response to the Chirp15 stimulus under baseline condition (blue) and after blocking KA channels (orange), using BaCl2 (top) and 3,4-DAP (bottom), respectively. (c) Impedance amplitude plotted as functions of input current frequency derived from corresponding color-matched traces shown in (b), under baseline condition (blue) and after blocking KA channels (orange) using BaCl2 (top) or 3,4-DAP (bottom). (d,e) Population data (also depicted as quartiles) for the effect of blocking KA channels, using BaCl2 (d) or 3,4-DAP (e), on resonance frequency (fR) for the three sub-populations of recording locations. *p < 0.05 Mann Whitney U test. (f) Cumulative probability of percentage change in fR in response to blocking A-type K+ channels using BaCl2 (top) or 3,4-DAP (bottom). (g) Population data for percentage change in fR after blocking KA channels, using either BaCl2 (left) or 3,4-DAP (right), plotted as a function of recording location. Open circles represent individual cells and filled circles represent the average values (mean ± SEM).
Mentions: Computational models have predicted that KA channels, despite being fast transient channels, could alter low-frequency spectral tuning in CA1 pyramidal neuron somata and their dendrites27. To test this prediction, we measured the responses of soma or dendrites to a chirp current (0–15 Hz in 15 s; Fig. 1c) stimulus before and after blocking KA channels (Figs 1 and 4b). Quantifying frequency-dependent response properties of neurons from the voltage responses to the chirp stimulus (Fig. 4c), we found that blocking KA channels resulted in a decrease in resonance frequency, fR, across the somato-apical trunk (Fig. 4d,e) (Tables S1 and S2), with percentage changes not significantly different across the somato-apical trunk (Fig. 4f,g, BaCl2: p = 0.28 and 3,4-DAP: p = 0.43 Kruskal-Wallis rank sum test).

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