Spatial heterogeneity of intracellular Ca2+ signals in axons of basket cells from rat cerebellar slices

1. Using tight-seal whole-cell recording and digital fluorescence imaging, we studied intracellular calcium (ca(i)(2+)) dynamics in cerebellar basket cells, whose dendrites, axon and presynaptic terminals are coplanar, an optimal configuration for simultaneous optical measurements of all functional domains. 2. In Cs+-loaded neurones, depolarizing pulses induced large Ca-i(2+) transients in single axonal varicosities and synaptic terminals, contrasting with much weaker signals between varicosities or in the somato-dendritic domain. 3. Axonal branch points consistently displayed [Ca2+](i) rises of similar magnitude and time course to those in axonal terminals and varicosities. 4. In biocytin-filled basket cells, varicosity-like swellings were present along the axon including its branch points. Thus, axonal enlargements are not due to fluorescence-induced cell damage. 5. The spatial heterogeneity of Ca-i(2+) signals was also observed in Kf-loaded cells upon depolarizing trains, suggesting that this behaviour is an intrinsic property of Ca-i(2+) homeostasis in basket cells. 6. We conclude that depolarization of basket cell axons evokes high local Ca-i(2+) signals in synaptic terminals, en passant varicosities and branch points. While high [Ca2+](i) in presynaptic structures presumably triggers transmitter release, Ca-i(2+) transients at branch points may control signal transmission in the axonal arborization.