Components of action potential repolarization in cerebellar parallel fibres

Key points The presynaptic action potential waveform was investigated in cerebellar parallel fibres from rats. The spike repolarization was composed of a fast tetraethylammonium‐sensitive component and a slow margatoxin‐sensitive depolarized after‐potential (DAP). These components could be manipulated relatively independently, possibly offering independent control of synchronous and asynchronous transmitter release. Axonal electrical activation sometimes gave bursts of action potentials at the soma; these bursts were created by the axon because they invaded the soma at membrane potentials well below the somatic spike threshold. Axonal bursts could reliably be induced by increasing the DAP pharmacologically, suggesting that proper control of DAP amplitude is necessary to suppress axonal bursting. The fast repolarization was particularly well controlled because blockers of three groups of K+ channels (tetraethylammonium, margatoxin and quinine) were needed to abolish it.AbstractRepolarization of the presynaptic action potential is essential for transmitter release, excitability and energy expenditure. Little is known about repolarization in thin, unmyelinated axons forming en passant synapses, which represent the most common type of axons in the mammalian brain's grey matter. We used rat cerebellar parallel fibres, an example of typical grey matter axons, to investigate the effects of K+ channel blockers on repolarization. We show that repolarization is composed of a fast tetraethylammonium (TEA)‐sensitive component, determining the width and amplitude of the spike, and a slow margatoxin (MgTX)‐sensitive depolarized after‐potential (DAP). These two components could be recorded at the granule cell soma as antidromic action potentials and from the axons with a newly developed miniaturized grease‐gap method. A considerable proportion of fast repolarization remained in the presence of TEA, MgTX, or both. This residual was abolished by the addition of quinine. The importance of proper control of fast repolarization was demonstrated by somatic recordings of antidromic action potentials. In these experiments, the relatively broad K+ channel blocker 4‐aminopyridine reduced the fast repolarization, resulting in bursts of action potentials forming on top of the DAP. We conclude that repolarization of the action potential in parallel fibres is supported by at least three groups of K+ channels. Differences in their temporal profiles allow relatively independent control of the spike and the DAP, whereas overlap of their temporal profiles provides robust control of axonal bursting properties.