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The Journal of Neuroscience, September 24, 2008, 28(39):9710-9722; doi:10.1523/JNEUROSCI.1955-08.2008

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Behavioral/Systems/Cognitive
Precise and Fuzzy Coding by Olfactory Sensory Neurons

Derek J. Hoare, Catherine R. McCrohan, and Matthew Cobb

Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, United Kingdom

Correspondence should be addressed to Matthew Cobb at the above address. Email: cobb{at}manchester.ac.uk

The exact nature of the olfactory signals that arrive in the brain from the periphery, and their reproducibility, remain essentially unknown. In most organisms, the sheer number of olfactory sensory neurons (OSNs) makes it impossible to measure the individual responses of the entire population. We measured the individual in situ electrophysiological activity of OSNs in Drosophila larvae, in response to stimulation with 10 aliphatic odors (alcohols and esters). We studied control larvae (a total of 296 OSNs) and larvae with a single functional OSN, created using the Gal4-upstream activator sequence system. Most OSNs showed consistent, precise responses (either excitation or inhibition) in response to a given odor. Some OSNs also showed qualitatively variable responses ("fuzzy coding"). This robust variability was an intrinsic property of these neurons: it was not attributable to odor type, concentration, stimulus duration, genotype, or interindividual differences, and was seen in control larvae and in larvae with one and two functional OSNs. We conclude that in Drosophila larvae the peripheral code combines precise coding with fuzzy, stochastic responses in which neurons show qualitative variability in their responses to a given odor. We hypothesize that fuzzy coding occurs in other organisms, is translated into differing degrees of activation of the glomeruli, and forms a key component of response variability in the first stages of olfactory processing.

Key words: olfaction; Drosophila; larvae; electrophysiology; coding; periphery

Received Jan. 13, 2008; revised Aug. 7, 2008; accepted Aug. 18, 2008.

Correspondence should be addressed to Matthew Cobb at the above address. Email: cobb{at}manchester.ac.uk


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