Coincident stimulation with pheromone components improves temporal pattern resolution in central olfactory neurons.

Abstract

Male moths must detect and resolve temporal discontinuities in the sex pheromonal odor signal emitted by a conspecific female moth to orient to and locate the odor source. We asked how sensory information about two key components of the pheromone influences the ability of certain sexually dimorphic projection (output) neurons in the primary olfactory center of the male moth's brain to encode the frequency and duration of discrete pulses of pheromone blends. Most of the male-specific projection neurons examined gave mixed postsynaptic responses, consisting of an early suppressive phase followed by activation of firing, to stimulation of the ipsilateral antenna with a blend of the two behaviorally essential pheromone components. Of 39 neurons tested, 33 were excited by the principal (most abundant) pheromone component but inhibited by another, less abundant but nevertheless essential component of the blend. We tested the ability of each neuron to encode intermittent pheromonal stimuli by delivering trains of 50-ms pulses of the two-component blend at progressively higher rates from 1 to 10 per second. There was a strong correlation between 1) the amplitude of the early inhibitory post-synaptic potential evoked by the second pheromone component and 2) the maximal rate of odor pulses that neuron could resolve (r = 0.92). Projection neurons receiving stronger inhibitory input encoded the temporal pattern of the stimulus with higher fidelity. With the principal, excitatory component of the pheromone alone as the stimulus, the dynamic range for encoding stimulus intermittency was reduced in nearly 60% of the neurons tested. The greatest reductions were observed in those neurons that could be shown to receive the strongest inhibitory input from the second behaviorally essential component of the blend. We also tested the ability of these neurons to encode stimulus duration. Again there was a strong correlation between the strength of the inhibitory input to a neuron mediated by the second pheromone component and that neuron's ability to encode stimulus duration. Neurons that were strongly inhibited by the second component could accurately encode pulses of the blend from 50 to 500 ms in duration (r = 0.94), but that ability was reduced in neurons receiving little or no inhibitory input (r = 0.23). This study confirms that certain olfactory projection neurons respond optimally to a particular odor blend rather than to the individual components of the blend. The key components activate opposing synaptic inputs that enable this subset of central neurons to copy the duration and frequency of intermittent odor pulses that are a fundamental feature of airborne olfactory stimuli.