Temporal tuning of odor responses in pheromone-responsive projection neurons in the brain of the sphinx moth Manduca sexta

By means of intracellular recording and staining, we studied the ability of several distinct classes of projection (output) neurons, which innervate t he sexually dimorphic macroglomerular complex (MGC-PNs) in the antennal lob e of the male moth Manduca sexta, to encode naturally intermittent sex pher omonal stimuli. In many MGC-PNs, antennal stimulation with a blend of the t wo essential pheromone components evoked a characteristic triphasic respons e consisting of a brief, hyperpolarizing inhibitory potential (I-1) followe d by depolarization with firing of action potentials and then a delayed per iod of hyperpolarization (I-2). MGC-PNs described in this study resolved pu lsed pheromonal stimuli, up to about five pulses/second, with a distinct bu rst of action potentials for each pulse of odor. The larger the amplitude o f I-1, the higher the pulse rate an MGC-PN could follow illustrating the im portance of inhibitory synaptic input in shaping the temporal firing proper ties of these glomerular output neurons. In some MGC-PNs, triphasic respons es were evoked by antennal stimulation with only one of the two key pheromo ne components. Again, the maximal pulse rate that an MGC-PN could follow wi th that pheromone component as sole stimulus was high in MGC-PNs that respo nded with a strong I-1. These component-specific MGC-PNs innervated only on e of the two principal glomeruli of the MGC, while MGC-PNs that were primar ily excited by antennal stimulation with either key pheromone component had arborizations in both major MGC glomeruli. These observations therefore su ggest that the population of antennal olfactory receptor cells responding t o a single pheromone component is functionally heterogeneous: a subset of t hese sensory cells activates the excitatory drive to many uniglomerular MGC -PNs, while others feed onto inhibitory circuits that hyperpolarize the sam e PNs. This convergence of opposing inputs is a circuit property common to uniglomerular MGC-PNs branching in either of the major MGC glomeruli, and i t enhances the ability of these glomerular output neurons to resolve interm ittent olfactory input. Synaptic integration at the uniglomerular PN level thus contributes to the transmission of behaviorally important temporal inf ormation about each key pheromone component to higher centers in the brain. (C) 1999 Wiley-Liss, Inc.