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The Journal of Neuroscience, November 19, 2008, 28(47):12523-12534; doi:10.1523/JNEUROSCI.2715-08.2008

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Behavioral/Systems/Cognitive
Inhibition Shapes Sex Selectivity in the Mouse Accessory Olfactory Bulb

Rebecca C. Hendrickson, Sandra Krauthamer, James M. Essenberg, and Timothy E. Holy

Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri, 63130

Correspondence should be addressed to Rebecca C. Hendrickson or Timothy E. Holy, Campus Box 8108, 660 S. Euclid Avenue, St. Louis, MO 63130. Email: chendrickson{at}wustl.edu and Email: holy{at}wustl.edu, respectively

Laterally connected inhibitory circuitry is found throughout the nervous system, including many early sensory processing systems. The extent to which it plays a role in shaping neuronal stimulus selectivity in systems like olfaction, however, which lack a simple two-dimensional representation of their stimulus space, has remained controversial. We examined this issue using an experimental preparation that allowed electrophysiological recording from the accessory olfactory bulb of an anesthetized mouse during the controlled delivery of pheromonal stimuli, in this case derived from the urine of male and female mice. We found that individual neurons were often highly selective for the sex of the urine donor. Examination of both explicitly inhibitory responses, as well as responses to mixtures of male and female urine, revealed that laterally connected inhibition was both prevalent and of large magnitude, particularly for male-selective neurons. Pharmacological manipulation of this inhibition resulted in a shift in many neurons' stimulus selectivities. Finally, we found that a behavioral response (pregnancy block) evoked by the presence of unfamiliar male urine could be suppressed by the addition of female urine to the stimulus, demonstrating that this system displays a behavioral opponency consistent with neural inhibition. Together, these results indicate that laterally connected inhibitory circuitry in the accessory olfactory bulb plays an important role in shaping neural selectivity for natural stimuli.

Key words: lateral inhibition; olfaction; accessory olfactory bulb; pheromone; pregnancy block; sex differences

Received June 13, 2008; revised Sept. 18, 2008; accepted Oct. 10, 2008.

Correspondence should be addressed to Rebecca C. Hendrickson or Timothy E. Holy, Campus Box 8108, 660 S. Euclid Avenue, St. Louis, MO 63130. Email: chendrickson{at}wustl.edu and Email: holy{at}wustl.edu, respectively
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