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Back-propagating action potentials mediate calcium signalling in dendrites of bitufted interneurons in layer 2/3 of rat somatosensory cortex

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Kaiser,  Katharina
Department of Cell Physiology, Max Planck Institute for Medical Research, Max Planck Society;

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Zilberter,  Yuri
Department of Cell Physiology, Max Planck Institute for Medical Research, Max Planck Society;

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Sakmann,  Bert
Department of Cell Physiology, Max Planck Institute for Medical Research, Max Planck Society;

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Citation

Kaiser, K., Zilberter, Y., & Sakmann, B. (2001). Back-propagating action potentials mediate calcium signalling in dendrites of bitufted interneurons in layer 2/3 of rat somatosensory cortex. Journal of Physiology, 535(1), 17-31. doi:10.1111/j.1469-7793.2001.t01-1-00017.x.


Cite as: https://hdl.handle.net/11858/00-001M-0000-0028-F086-A
Abstract
1. Bitufted interneurons in layer 2/3 of the rat (P14) somatosensory cortex have elongated apical and basal dendritic arbors that can span the entire depth of the cortex. Simultaneous dendritic and somatic whole-cell voltage recordings combined with Ca2+ fluorescence measurements were made to quantify voltage and Ca2+ signalling in dendritic arbors of bitufted neurons. 2. Action potentials (APs) initiated close to the soma by brief current injection back-propagated into the apical and basal dendritic arbors and evoked a transient increase in volume-averaged dendritic Ca2+ concentration (Delta[Ca(2+)](i)) of about 140 nM peak amplitude per AP. The AP evoked Ca2+ signal decayed with a time constant of about 200 ms. 3. A relatively high endogenous Ca(2+) binding ratio of approximately 285 determines the comparatively small rise in [Ca(2+)](i) of bitufted cell dendrites evoked by a back-propagating AP. 4. The [Ca(2+)](i) transient evoked by back-propagating dendritic APs decreased with distance (< or = 50 microm) from the soma in some neurons. At distances greater than 50 microm transients did not show a spatial gradient between the proximal and distal dendritic branches. 5. During trains of APs the mean amplitude of the steady-state increase in dendritic [Ca(2+)](i) encoded the AP frequency linearly up to 40 Hz with a slope of 20 nM Hz(-1). 6. The results suggest that APs initiated in the axon of bitufted neurons back-propagate and 'copy' the pattern of the axon's electrical activity also to the dendritic arbor. The AP pattern is transduced into a transient rise of dendritic [Ca(2+)](i) which, presumably, can regulate the receptive properties of the dendritic arbor for synaptic input. 7. Bitufted interneurons in layer 2/3 of the rat (P14) somatosensory cortex have elongated apical and basal dendritic arbors that can span the entire depth of the cortex. Simultaneous dendritic and somatic whole-cell voltage recordings combined with Ca2+ fluorescence measurements were made to quantify voltage and Ca2+ signalling in dendritic arbors of bitufted neurons. 8. Action potentials (APs) initiated close to the soma by brief current injection back-propagated into the apical and basal dendritic arbors and evoked a transient increase in volume-averaged dendritic Ca2+ concentration (Delta[Ca(2+)](i)) of about 140 nM peak amplitude per AP. The AP evoked Ca2+ signal decayed with a time constant of about 200 ms. 9. A relatively high endogenous Ca2+ binding ratio of approximately 285 determines the comparatively small rise in [Ca(2+)](i) of bitufted cell dendrites evoked by a back-propagating AP. 10. The [Ca(2+)](i) transient evoked by back-propagating dendritic APs decreased with distance (< or = 50 microm) from the soma in some neurons. At distances greater than 50 microm transients did not show a spatial gradient between the proximal and distal dendritic branches. 11. During trains of APs the mean amplitude of the steady-state increase in dendritic [Ca(2+)](i) encoded the AP frequency linearly up to 40 Hz with a slope of 20 nM Hz(-1). 12. The results suggest that APs initiated in the axon of bitufted neurons back-propagate and also 'copy' the pattern of the axon's electrical activity to the dendritic arbor. The AP pattern is transduced into a transient rise of dendritic [Ca(2+)](i) which, presumably, can regulate the receptive properties of the dendritic arbor for synaptic input.