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The Journal of Neuroscience, November 12, 2008, 28(46):11989-11997; doi:10.1523/JNEUROSCI.3106-08.2008

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Behavioral/Systems/Cognitive
Compensatory Rapid Switching of Binasal Inputs in the Olfactory Cortex

Shu Kikuta,^1,2 Hideki Kashiwadani,¹ and Kensaku Mori¹

Departments of ¹Physiology and ²Otolaryngology, Graduate School of Medicine, The University of Tokyo, Tokyo 113-0033, Japan

Correspondence should be addressed to Kensaku Mori, Department of Physiology, Graduate School of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan. Email: moriken{at}m.u-tokyo.ac.jp

Odors are inhaled through the nostrils into two segregated nasal passages and detected by sensory neurons in the bilateral olfactory epithelia. Airflow through the two nasal passages is usually asymmetrical because of alternating changes in nasal mucosal congestion. Here we show that neurons in the anterior olfactory nucleus (AON) of the adult rat olfactory cortex are ordinarily dominated by ipsi-nasal inputs and that binasal neurons in the AON respond to ipsilateral and contralateral nasal inputs with nearly equivalent odorant category selectivity. Deprivation of ipsilateral nasal inputs by unilateral nostril obstruction greatly enhanced the response to contralateral odor stimulation, in a reversible manner, in 33% of AON neurons within only several minutes. In 27% of AON neurons that showed spike responses induced by the inspiration of room air, ipsilateral nasal obstruction initially suppressed respiration phase-locked spike discharges and, several minutes later, induced respiration phase-locked discharges with longer delays between inspiration and response. Recordings from AON neurons in rats with anterior commissure (AC) transection indicated that the resumed respiration phase-locked discharges with longer delays were mediated by the contralateral pathway via the AC. The ipsi-nasal occlusion-induced switching of nasal inputs to individual AON neurons shows that a subset of AON neurons in the adult rat has neuronal mechanisms for rapid nostril dominance plasticity, which may enable both right and left olfactory cortices to preserve their responsiveness to the external odor world, despite reciprocal changes in nasal airflow.

Key words: olfactory cortex; anterior olfactory nucleus; nostril obstruction; binasal inputs; compensation; homeostatic plasticity

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Received June 27, 2008; revised Aug. 18, 2008; accepted Oct. 4, 2008.

Correspondence should be addressed to Kensaku Mori, Department of Physiology, Graduate School of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan. Email: moriken{at}m.u-tokyo.ac.jp

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