Dendritic calcium accumulation regulates wind sensitivity via short-term depression at cercal sensory-to-giant interneuron synapses in the cricket

An in vivo Ca²⁺ imaging technique was applied to examine the cellular mechanisms for attenuation of wind sensitivity in the identified primary sensory interneurons in the cricket cercal system. Simultaneous measurement of the cytosolic Ca²⁺ concentration ([Ca²⁺]_i) and membrane potential of a wind-sensitive giant interneuron (GI) revealed that successive air puffs caused the Ca²⁺ accumulation in dendrites and diminished the wind-evoked bursting response in the GI. After tetanic stimulation of the presynaptic cercal sensory nerves induced a larger Ca²⁺ accumulation in the GI, the wind-evoked bursting response was reversibly decreased in its spike number. When hyperpolarizing current injection suppressed the [Ca²⁺]_i elevation during tetanic stimulation, the wind-evoked EPSPs were not changed. Moreover, after suprathreshold tetanic stimulation to one side of the cercal nerve resulted in Ca²⁺ accumulation in the GI's dendrites, the slope of EPSP evoked by presynaptic stimulation of the other side of the cercal nerve was also attenuated for a few minutes after the [Ca²⁺]_i had returned to the prestimulation level. This short-term depression at synapses between the cercal sensory neurons and the GI (cercal-to-giant synapses) was also induced by a depolarizing current injection, which increased the [Ca²⁺]_i, and buffering of the Ca²⁺ rise with a high concentration of a Ca²⁺ chelator blocked the induction of short-term depression. These results indicate that the postsynaptic Ca²⁺ accumulation causes short-term synaptic depression at the cercal-to-giant synapses. The dendritic excitability of the GI may contribute to postsynaptic regulation of the wind-sensitivity via Ca²⁺-dependent depression.