Temporal Representations of Odors in an Olfactory Network

Abstract

The responses of projection neurons in the antennal lobe of the locust brain (the functional analog of mitral–tufted cells in the vertebrate olfactory bulb) to natural blends and simple odors were studied with multiple intra- and extracellular recordings in vivo. Individual odors evoked complex temporal response patterns in many neurons. These patterns differed across odors for a given neuron and across neurons for a given odor, but were stable for each neuron over repeated presentations (separated by seconds to minutes) of the same odor. The response of individual neurons to an odor was superimposed on an odor-specific coherent oscillatory population activity. Each neuron usually participated in the coherent oscillations during one or more specific epochs of the ensemble activity. These epochs of phase locking were reliable for each neuron over tens of repeated presentations of one odor. The timing of these epochs of synchronization differed across neurons and odors. Correlated activity of specific pairs of neurons, hence, generally occurred transiently during the population response, at times that were specific to these pairs and to the odor smelled. The field potential oscillations, therefore, fail to reveal a progressive transformation of the synchronized ensemble as the response to the odor unfolds. We propose that (1) odors are represented by spatially and temporally distributed ensembles of coherently firing neurons, and (2) the field potential oscillations that characterize odor responses in the olfactory system occur, at least in this animal, in parallel with a slower dynamic odor representation.