ACTION POTENTIAL SIGNALING AT THE MORPHO-FUNCTIONALLY DIVERSE AXON TERMINALS OF HIPPOCAMPAL MOSSY FIBERS
Hippocampal mossy fibers (axons of granule cells, MFs) carry structurally and functionally heterogeneous synapses. Large boutons (LMFBs) form facilitating connections with CA3 pyramidal cells, whereas the more numerous small terminals (sMFBs) excite GABAergic cells with heterogeneous release probability. Because action potential (AP) dynamics have been proposed to contribute to the characteristic facilitation at the LMFB, we compared their electrical behavior with sMFBs to understand the role of local intrinsic axonal signaling in different physiological functions of the boutons of the same axon. First we performed direct patch-clamp recordings from sMFBs, LMFBs and axonal shafts. AP shapes and their activity-dependent broadening were similar in all MF structures regardless of their different functions. Outside-out patch recordings revealed that all of them (including axonal shafts) have substantial amount of sodium and potassium currents, supporting the local regulation of the firing properties. Then, we used voltage imaging (JPW1114 at 10 kHz) to follow the AP dynamics in different MF compartments simultaneously. The optically recorded APs showed similar average activity-induced broadening in all MF segments confirming our direct patch-clamp measurements. AP dynamics at the filopodial boutons were strongly coupled to the spiking behavior of its parent LMFB. However, the AP shape in the main axon was uncoupled from the AP dynamics of proximal LMFBs. Altogether, the results show that functionally different MF compartments along the main axon have similar local ionic mechanisms that support fast axonal signaling and allow the local regulation of the firing dynamics.