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Neurons in the Anterior Olfactory Nucleus Pars Externa Detect Right Or Left Localization of Odor Sources

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Neurons in the Anterior Olfactory Nucleus Pars Externa Detect Right Or Left Localization of Odor Sources Neurons in the anterior olfactory nucleus pars externa detect right or left localization of odor sources Shu Kikutaa,b,c, Kenichiro Satob, Hideki Kashiwadanib,c, Koichi Tsunodad, Tatsuya Yamasobaa, and Kensaku Morib,c,1 Departments of aOtolaryngology and bPhysiology, Graduate School of Medicine, University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan; dDepartment of Artificial Organs and Medical Device Creation, National Institute of Sensory Organs, Tokyo Medical Center, National Hospital Organization, Meguro-ku, Tokyo 152-8902, Japan; and cJapan Science and Technology Agency, Core Research for Evolutional Science and Technology, Tokyo 113-0033, Japan Edited by John G. Hildebrand, University of Arizona, Tucson, AZ, and approved June 2, 2010 (received for review March 26, 2010) Rodents can localize odor sources by comparing odor inputs to the the ipsilateral OB (8–11). In addition, AON neurons receive in- right and left nostrils. However, the neuronal circuits underlying puts from the contralateral olfactory cortex via the anterior com- such odor localization are not known. We recorded neurons in the missure (12, 13), suggesting that individual AON neurons receive anterior olfactory nucleus (AON) while administering odors to odor information originating from both ipsilateral and contralat- the ipsilateral or contralateral (ipsi- or contra-) nostril. Neurons in eral OEs. The AON is composed of two separate structures, the the AON pars externa (AONpE) showed respiration phase-locked pars principalis (AONpP) and pars externa (AONpE) (12). excitatory spike responses to ipsinostril-only stimulation with a We report here that AONpE neurons show ipsilateral (ipsi)- category of odorants, and inhibitory responses to contranostril-only nostril excitation and contralateral (contra)-nostril inhibition (E- stimulation with the same odorants. Simultaneous odor stimulation I) responses, and compare the magnitude of responses to ipsino- of the ipsi- and contranostrils elicited significantly smaller responses stril odor inputs with those of contranostril inputs. than ipsinostril-only stimulation, indicating that AONpE neurons subtract the contranostril odor inputs from ipsinostril odor inputs. Results An ipsilateral odor source induced larger responses than a centrally We recorded single-unit spike responses of individual AON neu- located source, whereas an odor source at the contralateral position rons in urethane-anesthetized rats in response to nasal stimulation elicited inhibitory responses. These results indicate that individual with a panel of odors consisting of 10 categories of odorant mol- AONpE neurons can distinguish the right or left position of an odor ecules, each containing five separate odorants (Fig. 1A and Table source by referencing signals from the two nostrils. S1). A thermoplastic external nasal septum that fitted the external shape of the rat nose was used to prevent odors delivered in front olfactory cortex | binasal inputs | odor localization of one nostril from spreading to the contralateral nostril (Fig. 1A), which enabled the selective stimulation of either the ipsilateral or lfactory neuronal circuits translate odor cues into a variety of contralateral olfactory epithelium (6). We examined spike re- Obehavioral responses that enable rodents to find and locate sponses of individual neurons in the rostral part of the AON (Fig. food, mates, and predators. For the directional localization of 1B) to ipsinostril-only and contranostril-only stimulation with the sound sources, the central auditory system has neuronal circuit panel of odorants (52 cells in 36 rats). AON neurons that showed mechanisms that compare auditory inputs from the right and left excitatory spike responses to ipsinostril stimulation with an odor- cochleas (1). Similarly, rodents can localize odor sources by com- ant category showed three types of responses to contranostril paring odor inputs through the right and left nostrils (2). How- stimulation with the same odorant category: excitatory responses ever, the neuronal circuits and mechanisms subserving the right or (ipsi-excitatory and contraexcitatory response, or an E-E-type left localization of odor sources are not yet known. response), no response (ipsi-excitatory and contranull response, In the auditory system, binaural sound localization relies on E-0-type response), and suppressive responses (ipsi-excitatory and central neuronal mechanisms that compare auditory inputs from contrainhibitory response, E-I-type response) (6). the two ears. Interaural differences in the intensity of the sound pre- Individual AON neurons that showed E-I responses to ipsi- and ssure level arriving at the two ears are important cues used by the contranostril stimulation with one odorant category did not show mammalian auditory system to localize higher-frequency sounds E-I responses to the other odorant categories (Fig. 2), suggesting (3). Neurons in the lateral superior olive are sensitive to interaural that their E-I response is specific to a single odorant category. In intensity differences, being excited by stimulation of the ipsilateral addition, these AON neurons did not show E-E-type responses to ear and suppressed by stimulation of the contralateral ear (4). These any of the 10 odorant categories (Fig. 2). We thus classified these neurons are thus referred to as ipsi-excitation and contrainhibition neurons as single-category E-I-type neurons. Because we prefer- (E-I) neurons and play a key role in sound source localization (5). entially searched for E-I-type neurons, we analyzed 31 E-I-type Odorants are inhaled through the two nostrils into two segre- neurons, 13 E-E-type neurons, and 8 E-0-type neurons. Fig. 1C gated nasal passages. Because the two passages are relatively well shows a representative example of a single-category E-I-type AON isolated, odorants inhaled through one nostril activate olfactory neuron. This cell showed high-frequency burst spike responses to sensory neurons only in the ipsilateral olfactory epithelium (6). ipsinostril stimulation with sulfide odorants and suppressive re- Therefore, to detect the right or left localization of odor sources, sponses to contranostril stimulation with the same odorants. Be- the central olfactory system needs only to compare afferent odor cause single-category E-I AON neurons are candidate neurons signals originating from the right and left olfactory epithelia (OEs). NEUROSCIENCE Olfactory sensory neurons in the epithelium project their axons to the ipsilateral olfactory bulb (OB), and mitral and tufted cells in the Author contributions: S.K. and K.M. designed research; S.K. performed research; S.K. and OB project their axons to the ipsilateral olfactory cortex (7). K.S. analyzed data; and S.K., K.S., H.K., K.T., T.Y., and K.M. wrote the paper. Therefore, odor signals originating from the right and left olfactory The authors declare no conflict of interest. sensory epithelia are largely segregated at the level of the right This article is a PNAS Direct Submission. and left OBs, and their afferents are segregated to the right or Freely available online through the PNAS open access option. left olfactory cortex. 1To whom correspondence should be addressed. E-mail: [email protected]. The anterior olfactory nucleus (AON) is the most rostral region This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. of the olfactory cortex and receives excitatory axonal inputs from 1073/pnas.1003999107/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1003999107 PNAS | July 6, 2010 | vol. 107 | no. 27 | 12363–12368 Downloaded by guest on October 2, 2021 A BD E C F Fig. 1. E-I-type neurons in the AON. (A) Experimental procedure used for uninostril odor stimulation. An external nasal septum was used to ensure delivery of odorants selectively to unilateral olfactory epithelium. Single-unit recordings were obtained from AON neurons. (B) Lateral view of a 3D reconstruction of the olfactory peduncle of a rat brain. AONpE (black); AONpP (green); MOB, main olfactory bulb; AOB, accessory olfactory bulb; NC, neocortex. (C) Spike responses of an E-I-type AON neuron to ipsinostril (Upper left trace) and contranostril (Upper right trace) odor stimulation. Resp., the trace of the respiration monitor. The ascending and descending phases of the trace indicate inspiration and expiration, respectively. Raster, raster representation of the spike responses. Each row corresponds to a single odor stimulation. Peristimulus time histograms of the response are shown at the bottom. Bar, duration of odor stimulation (sulfide category, 3 s). F.R., firing rate (Hz). (D) Locations of E-I type neurons in the AONpE. Dr, Di, Dc: rostral, intermediate, and caudal regions of the dorsal AONpE, respectively. Vr, Vi, Vc: rostral, intermediate and caudal regions of the ventral AONpE, respectively. D-R, dorso-rostral; V-C, ventro-caudal. Red and yellow dots represent individual E-I type neurons. Numbered cells correspond to those in Fig. 2. (E) A raster representation of the spike responses (Upper) and peristimulus time histograms (Lower) from a single cell. Black bar, duration of odor stimulation (sulfide category, 3 s). (F) Morphology of the E-I-type AON neuron whose responses are shown in E. The cell was labeled with biotinylated dextran amine by juxtacellular electroporation (SI Materials and Methods). This cell emitted an axon collateral (single arrowhead) that reached the superficial part of layer II of the AONpP. AC, anterior commissure (double arrowhead). subserving the
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