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Importance of Newly Generated Neurons in the Adult Olfactory Bulb for Odor Discrimination

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Importance of Newly Generated Neurons in the Adult Olfactory Bulb for Odor Discrimination Importance of newly generated neurons in the adult olfactory bulb for odor discrimination Gilles Gheusi*†, Harold Cremer‡, Heather McLean*, Genevie` ve Chazal‡, Jean-Didier Vincent*, and Pierre-Marie Lledo*§ *Centre National de la Recherche Scientifique, Institut Alfred Fessard, Avenue de la Terrasse, 91198 Gif-sur-Yvette Cedex, France; †Unite Propre de Recherche de l’Enseignement Superieur (UPRES)-A 7025, Universite´Paris XIII, 93430 Villetaneuse Cedex, France; and ‡Laboratoire de Ge´ne´ tique et Physiologie du De´veloppement, Institut de Biologie du De´veloppement de Marseille, Campus de Luminy, 13288 Marseille Cedex 9, France Communicated by D. Carleton Gajdusek, Centre National de la Recherche Scientifique, Gif-sur-Yvette, France, December 2, 1999 (received for review October 19, 1999) In adult rodents, neurons are continually generated in the subven- neurons; and (ii) periglomerular neurons that make synapses tricular zone of the forebrain, from where they migrate tangen- onto the primary dendrites of mitral or tufted cells (see review tially toward the olfactory bulb, the only known target for these in ref. 14). neuronal precursors. Within the main olfactory bulb, they ascend Inhibitory synapses of such local interneurons from the olfac- radially into the granule and periglomerular cell layers, where they tory bulb and the antennal lobe in insects (the analogue of the differentiate mainly into local interneurons. The functional conse- vertebrate olfactory bulb) shape the temporal patterns of output quences of this permanent generation and integration of new neurons, namely, the mitral cells in vertebrates and the projec- neurons into existing circuits are unknown. To address this ques- tion neurons in insects (15–17). This temporal coding is thought tion, we used neural cell adhesion molecule-deficient mice that to be responsible for the synchronization of output neurons, and have documented deficits in the migration of olfactory-bulb neu- it has been demonstrated that synchronization is crucial for odor ron precursors, leading to about 40% size reduction of this struc- processing (refs. 18 and 19; see review in ref. 20). Thus, if granule ture. Our anatomical study reveals that this reduction is restricted cells produced in adulthood are necessary for olfactory bulb to the granule cell layer, a structure that contains exclusively function, then a defect in the rostral migration leading to a ␥ -aminobutyric acid (GABA)ergic interneurons. Furthermore, mu- reduction of the recruitment of new bulbar interneurons should tant mice were subjected to experiments designed to examine the alter olfactory behavioral responses. We have tested this hy- NEUROBIOLOGY behavioral consequences of such anatomical alteration. We found pothesis, first, by quantifying the level of migration and the size that the specific reduction in the newly generated interneuron of interneuron populations in NCAM-mutant mice and, second, population resulted in an impairment of discrimination between by investigating their olfactory performance. We found that the odors. In contrast, both the detection thresholds for odors and dramatic reduction in granule cells in knockout mice was short-term olfactory memory were unaltered, demonstrating that accompanied by impaired odor discrimination but not by im- a critical number of bulbar granule cells is crucial only for odor pairments in olfactory detection level or memory, indicating a discrimination but not for general olfactory functions. specific role for this cell population for downstream coding of odorant information. cell adhesion molecules ͉ neurogenesis ͉ interneurons ͉ ␥-aminobutyric acid (GABA) Materials and Methods Animals. Male NCAM-mutant mice used in this study were he olfactory bulb is one of the few structures in the mam- generated by Cremer et al. (12). All experiments were performed Tmalian central nervous system in which there is a continued ‘‘blind’’ to genotype on mice (C57BL͞6J) between 10 and 14 supplied of newly generated neurons (1–4). These progenitor months of age. Adult mice were kept under a 12-h light–dark cells originate from the subventricular zone of the lateral cycle with lights on at 08:00 and with food and water ad libitum. ventricle, which produces a proliferative population of stem cells A week before the start of behavioral experiments, mice were throughout the life of the animal (5). Their progeny can undergo housed singly in 60 ϫ 40 ϫ 20 cm polycarbonate cages. All of the cell death (6) or give rise to neuronal progenitors that migrate experiments were performed according to the principles of through a tangential pathway, called the rostral migratory laboratory animal care published by the French Regulation (51). stream, into the core of the main olfactory bulb (7, 8). Here, the precursor cells turn radially to invade the granule and periglo- Cytological and Immunohistological Analyses. Control and mutant merular layers, where they differentiate mainly into local inter- mice were deeply anesthetized with xylazine͞ketamine and neurons (2, 9). Although this ongoing neurogenesis, as well as the intracardially perfused with a solution of 4% paraformaldehyde migration process, has been extensively characterized, its func- in phosphate buffer (PB). The brain was dissected out and tional consequences remain unknown. immersed overnight in the same fixative at 4°C. Coronal and The tangential migration of precursors from the cells in the sagittal sections were serially cut at 40 ␮m using a Vibratome subventricular zone into the olfactory bulb is associated with the 1000 (TPI, St. Louis, MO). Immunohistochemistry was per- expression of the neural cell adhesion molecule (NCAM) in its formed on floating Vibratome sections as described previously highly polysialylated form (10). Hence, NCAM-knockout mice, (21, 22). Briefly, sections were first incubated overnight at 4°C which also have been shown to be almost totally devoid of ␥ polysialic acid, show a defect in the rostral migration of subven- with anti-glutamic acid decarboxylase (GAD)67 or anti- - tricular zone precursors, resulting in an accumulation of pre- aminobutyric acid (GABA) mAb (Sigma) before incubation cursors along the pathway and finally in a size reduction of the with the corresponding fluorescent-labeled or biotinylated sec- olfactory bulb (11, 12). A similar defect is observed in neonatal animals treated with an enzyme that specifically cleaves off the Abbreviations: GCL, granule cell layer; NCAM, neural cell adhesion molecules; GABA, polysialic acid moiety from NCAM (13). From these findings, it ␥-aminobutyric acid. was inferred that these alterations concern two classes of local §To whom reprint requests should be addressed. E-mail: [email protected]. inhibitory interneurons in the main olfactory bulb: (i) granule The publication costs of this article were defrayed in part by page charge payment. This cells that impinge onto mitral or tufted cell secondary dendrites article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C. and that constitute, by far, the main target for the newly arriving §1734 solely to indicate this fact. PNAS ͉ February 15, 2000 ͉ vol. 97 ͉ no. 4 ͉ 1823-1828 Downloaded by guest on October 3, 2021 ondary antibody (Vector Laboratories). Sections were analyzed by using a standard Leitz confocal microscope and the comple- mentary software package. To estimate the total number of cells in olfactory bulbs, the number of cell bodies in Nissl-stained (0.5% cresyl violet) or immuno-stained sections was determined within a defined grid area (100 ϫ 100 ␮m). BrdUrd Labeling and Detection. To determine the quantity of adult-generated cells, 5-bromo-2Ј-deoxyuridine (BrdUrd, 10 mg͞ml; Sigma), a marker of DNA synthesis, was administered intraperitoneally in mice with ages between postnatal days 60 and 120 (50 mg͞kg of body weight in 0.07 M NaOH in 0.9% NaCl). Four injections were given over 2 days and animals were perfused 12 h after the last injection. Vibratome sections of the brains were processed for immunohistochemistry as described above. To denature DNA, sections were treated for 30 min at 37°C with 2 M HCl in PB containing 0.5% Triton X-100, then rinsed three times in sodium tetraborate buffer (0.1 M, pH 8.5) before incubation with anti-BrdUrd antibody (1:100; Dako). The anti-BrdUrd antibody was then revealed with a corresponding fluorescent-labeled secondary antibody, and only immuno- stained nuclei were numbered. Olfactory Discrimination. Odors were presented by placing a glass plate on the floor of the animal’s home cage. Twenty-five microliters of a solution of paprika (or cinnamon) and sterilized water were placed onto a filter paper (Whatman no. 1) on the glass plate. Odorant solutions (10Ϫ4) were freshly prepared before each experiment. We used a habituation-dishabituation task in which each mouse was presented with the first odor (paprika or cinnamon) on one side of the plate and with water (as control) on the other side for five successive 5-min trials separated by 15-min intervals. On the sixth trial, the mouse was Fig. 1. Histologic (Nissl) appearance of normal and mutant main olfactory exposed for 5 min to a different odor (cinnamon or paprika, bulbs in adult mice. Comparison of 40-␮m thick Vibratome coronal (A) and respectively) on one side of the plate and water on the other side sagittal (B) sections of olfactory bulbs from wild-type (NCAMϩ/ϩ) and knock- (23). The mouse was considered to be sniffing whenever it had out (NCAMϪ/Ϫ) mice, showing the decreased size of the granule cell layer in its nose 1 cm or less from the surface of the glass plate. the mutants. Arrows indicate the mitral cell layer. (C) Details of cresyl violet- stained granule cell layer showing the presence of striated aggregates of cells ϭ ␮ ␮ Olfactory Sensitivity. Mice were exposed to a glass plate on which only in control animals (arrows). (Scale bars 150 minA and B and 200 m in C.) an odor (paprika) was put on one side and water on the other one.
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