Noradrenergic modulation of dendrodendritic inhibition in the olfactory bulb

  • Jahr C
  • Nicoll R
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Abstract

The output of the olfactory bulb is governed by the interaction of synaptic potentials with the intrinsic conductances of mitral cells. While mitral cells often are considered as simple relay neurons, conveying activity in olfactory receptor cells to the piriform cortex, there is strong physiological and behavioral evidence that local synaptic interactions within the olfactory bulb modulate mitral cell discharges and facilitate odorant discrimination. Understanding the circuitry of the olfactory bulb is complicated by the fact that most dendrites in this region are both pre- and postsynaptic. Feedback inhibition is mediated through reciprocal dendrodendritic synapses between the secondary dendrites of mitral cells and GABAergic granule cells. Here we show that glutamate released from mitral cell dendrites also activates local N-methyl-D-aspartate (NMDA) autoreceptors, generating an inward tail current following depolarizing voltage steps. Autoreceptor-mediated self-excitation is calcium dependent, can be evoked by single action potentials in the presence of magnesium, and is graded with the number of spikes in a train. We find that dendrodendritic inhibition also is evoked by single action potentials but saturates rapidly during repetitive discharges. Self-excitation also underlies the prolonged afterdischarges apparent in mitral cells following potassium channel blockade. Both afterdischarges and autoreceptor-mediated tail currents persist in TTX, suggesting that they are produced by local rather than polysynaptic actions of glutamate. Blockade of NMDA autoreceptors with 2-amino-5-phosphonovaleric acid (APV) reduces the firing frequency within action potential cluster. The rapid kinetics of self-excitation suggests a functional role of NMDA autoreceptors in prolonging periods of phasic firing in mitral cells.

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