Action potential modulates Ca2+-dependent and Ca2+-independent secretion in a sensory neuron.
Neurotransmitter release normally requires calcium triggering. However, the somata of dorsal root ganglion (DRG) neurons possess a calcium-independent but voltage-dependent secretion (CIVDS) in addition to the classic calcium-dependent secretion (CDS). Here, we investigated the physiological role of CIVDS and the contributions of CIVDS and CDS induced by action potentials (APs) in DRG soma. Using membrane capacitance measurements, caged calcium photolysis, and membrane capacitance kinetics analysis, we demonstrated that AP-induced secretion had both CIVDS and CDS components. Following physiological stimuli, the dominant component of AP-induced secretion was either CIVDS for spontaneous firing or CDS for high-intensity stimuli. AP frequency modulates CDS-coupled exocytosis and CIVDS-coupled endocytosis but not CIVDS-coupled exocytosis and CDS-coupled endocytosis. Finally, CIVDS did not contribute to excitatory postsynaptic currents induced by APs in DRG presynaptic terminals in the spinal cord. Thus, CIVDS is probably an essential physiological component of AP-induced secretion in the soma. These findings bring novel insights into primary sensory processes in DRG neurons.
Zheng
Hui
H
Institute of Molecular Medicine, Peking University, Beijing, China.
Fan
Juan
J
Xiong
Wei
W
Zhang
Chen
C
Wang
Xiao-Bing
XB
Liu
Tao
T
Liu
Hong-Ju
HJ
Sun
Lei
L
Wang
Ye-Shi
YS
Zheng
Liang-Hong
LH
Wang
Bai-Ren
BR
Zhang
Claire Xi
CX
Zhou
Zhuan
Z
D000200:Action Potentials; D000818:Animals; D002118:Calcium / Q000378:metabolism*; D002462:Cell Membrane / Q000502:physiology; D002478:Cells, Cultured; D025802:Electric Capacitance; D004705:Endocytosis; D019706:Excitatory Postsynaptic Potentials; D005727:Ganglia, Spinal / Q000502:physiology*; D066298:In Vitro Techniques; D007700:Kinetics; D018377:Neurotransmitter Agents / Q000378:metabolism*; D018408:Patch-Clamp Techniques; D010782:Photolysis; D051381:Rats; D017208:Rats, Wistar; D011984:Sensory Receptor Cells / Q000378:metabolism*
D018377:Neurotransmitter Agents; D002118:Calcium