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Axon initial segment potassium channel density in cortical neurons

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There is a growing interest in estimating actual density ranges of Na+ channels in the very thin axon, especially in the action potential (AP) initiation zone, i.e., the axon initial segment (AIS, 20-50 microns away from the cell body). Both immunostaining studies and patch-clamp recordings indicated a relatively high density of Na+ channels in AIS of either pyramidal regular-spiking (RS) cells [1] or fast-spiking (FS) GABAergic interneurons [2, 3]. Here, we investigated potassium channel densities in AISs of both RS and FS cells in same recording conditions.

Our axonal recordings directly revealed that there is a very lower potassium density gK = 185.8±19 pS/µm2 N = 16) for the RS AIS while a higher gK (495.7±108 pS/µm2, N = 11) for FS AIS, see Figure 1A. For both the RS pyramidal cells and FS PV cells, partially blocking K+ channels by applying 4-AP broadened the spike duration and decreased the dV/dt ratio significantly (P < 0.05) (For RS cells: N = 5; For RS cells: N = 4). Interestingly, we observed that the AP dV/dt ratio is an exponentially decaying function of the spike duration for both RS- and FS-spikings (see Figure 1B), such that y = 0.12+0.16EXP((0.5-x)/0.2), where y represents the dV/dt ratio and × represents the AP duration. These observations suggest strongly that potassium channel density is one of the major intrinsic factors dominating the spike shape properties, especially half-height spike duration and dV/dt ratio.

Figure 1
figure1

A. The bar graph shows peak K+ conductance density recorded in axon initial segment of cells (16 recording axons for RS pyramidal cell, 11 for FS interneuron) by outside-out axon patch recording technique. B. Summary of the results from partially blocking K+ channels. The AP dV/dt ratio is an exponentially decaying function of the spike duration.

In sum, the significant difference in potassium channel density in axonal initial segment where action potentials are initiated may play a critical role in controlling action potential properties of both RS- and FS-spiking cells in nervous system by the same general biophysical rule. These results may be important for constructing computational models of different types of cortical neurons.

References

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    Hu W, Tian C, Li T, Yang M, Hou H, Shu Y: Distinct contributions of Na(v)1.6 and Na(v)1.2 in action potential initiation and backpropagation. Nat Neurosci. 2009, 12 (8): 996-1002.

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    Hu H, Jonas P: A supercritical density of Na(+) channels ensures fast signaling in GABAergic interneuron axons. Nat Neurosci. 2014, 17 (5): 686-693.

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    Li T, Tian C, Scalmani P, Frassoni C, Mantegazza M, Wang Y, Yang M, Wu S, Shu Y: Action potential initiation in neocortical inhibitory interneurons. PLoS Biol. 2014, 12 (9): e1001944-

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Acknowledgements

This project is funded by NNSF of China (31271170) and Eastern Scholar SHH1140004) at Shanghai Institutions of Higher Learning.

Author information

Correspondence to Yuguo Yu.

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Keywords

  • Cortical Neuron
  • Intrinsic Factor
  • Action Potential Duration
  • GABAergic Interneuron
  • Axon Initial Segment