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

Abstract

By means ofintracellular recording and staining, we studied the ability of several distinct classes of projection (output) neurons, which innervate the sexually dimorphic macroglomerular complex (MGC-PNs) in the antennal lobe of the male moth Manduca sexta, to encode naturally intermittent sex pheromonal stimuli. In many MGC-PNs, antennal stimulation with a blend of the two essential pheromone components evoked a characteristic triphasic response consisting of a brief, hyperpolarizing inhibitory potential (I1) followed by depolarization with firing of action potentials and then a delayed period of hyperpolarization (I2). MGC-PNs described in this study resolved pulsed pheromonal stimuli, up to about five pulses/second, with a distinct burst of action potentials for each pulse of odor. The larger the amplitude of I1, the higher the pulse rate an MGC-PN could follow, illustrating the importance of inhibitory synaptic input in shaping the temporal firing properties of these glomerular output neurons. In some MGC-PNs, triphasic responses were evoked by antennal stimulation with only one of the two key pheromone components. Again, the maximal pulse rate that an MGC-PN could follow with that pheromone component as sole stimulus was high in MGC-PNs that responded with a strong I1. These component-specific MGC-PNs innervated only one of the two principal glomeruli of the MGC, while MGC-PNs that were primarily excited by antennal stimulation with either key pheromone component had arborizations in both major MGC glomeruli. These observations therefore suggest that the population of antennal olfactory receptor cells responding to a single pheromone component is functionally heterogeneous: a subset of these sensory cells activates the excitatory drive to many uniglomerular MGC-PNs, while others feed onto inhibitory circuits that hyperpolarize the same PNs. This convergence of opposing inputs is a circuit property common to uniglomerular MGC-PNs branching in either of the major MGC glomeruli, and it enhances the ability of these glomerular output neurons to resolve intermittent olfactory input. Synaptic integration at the uniglomerular PN level thus contributes to the transmission of behaviorally important temporal information about each key pheromone component to higher centers in the brain.