Skip to main content
SpringerLink
Log in

Odor representation and discrimination in mitral/tufted cells of the rat olfactory bulb

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Extracellular single-unit responses to odorants with various properties were recorded from mitral/tufted cells over large areas of the olfactory bulb of anesthetized rats. Each cell was exposed to one stimulus set consisting of five different odorants each at five concentrations. The resulting concentration-response profiles were compared. All mitral/tufted cells examined responded to two or more odorants, and the largest proportion of the cells were sensitive to all five odorants. Cells unresponsive to all five odorants regardless of concentration were not observed. Mitral/tufted cells sensitive to all three of the odorants that are known to evoke maximal electro-olfactograms in different regions of the olfactory epithelium were distributed widely throughout the olfactory bulb. There were no significant differences in latencies of odor responses either across recording sites or across odorants. A comparison of the concentration-response profiles suggested that all of the mitral/tufted cells were equally capable of responding to any odorant with their own distinctive pattern, but that the cells tended to show an identical pattern rather than variable pattern of response to different odorants. Five mitral/tufted cells isolated within 800 μm of one electrode track showed different concentration-response profiles. Of 18 simultaneously recorded spike pairs with different amplitudes and discharge patterns recorded incidentally through one electrode at different sites, 10 had different and 8 had identical response patterns to odorants. These results suggest that: (1) mitral/tufted cells are sensitive to a broad spectrum of odorants, but respond with their own patterns to odorants; (2) odor discrimination is not uniform in neighboring cells, and a discrimination unit is comprised of a single cell.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Reference

  • Adrian ED (1950) Sensory discrimination with some recent evidence from the olfactory organ. Br Med Bull 6:330–333

    Google Scholar 

  • Astic L, Saucier D (1986) Anatomical mapping of the neuroepithelial projection to the olfactory bulb in the rat. Brain Res Bull 16:445–454

    Google Scholar 

  • Astic L, Saucier D, Holley A (1987) Topographical relationships between olfactory receptor cells and glomerular foci in the rat olfactory bulb. Brain Res 424:144–152

    Google Scholar 

  • Axel R (1995) The molecular logic of smell. Sci Am 273:130–137

    Google Scholar 

  • Boulet M, Daval G, Leveteau J (1978) Qualitative and quantitative odour discrimination by mitral cells as compared to anterior olfactory nucleus cells. Brain Res 142:123–134

    Google Scholar 

  • Buonviso N, Chaput MA (1990) Response similarity to odors in olfactory output cells presumed to be connected to the same glomerulus: electrophysiological study using simultaneous single-unit recordings. J Neurophysiol 63:447–454

    Google Scholar 

  • Chaput M, Holley A (1979) Spontaneous activity of olfactory bulb neurons in awake rabbits, with some observations on the effects of pentobarbital anaesthesia. J Physiol (Paris) 75:939–948

    Google Scholar 

  • Chess A, Buck L, Dowling MM, Axel R, Ngai J (1992) Molecular biology of smell: expression of the multigene family encoding putative odorant receptors. Cold Spring Harb Symp Quant Biol 57:505–516

    Google Scholar 

  • Cinelli AR, Hamilton KA, Kauer JS (1995) Salamander olfactory bulb neuronal activity observed by video rate, voltage-sensitive dye imaging. III. Spatial and temporal properties of responses evoked by odorant stimulation. J Neurophysiol 73:2053–2071

    Google Scholar 

  • Corrigall WA, Sherebrin MH (1976) Spontaneous activity in amphibian second-order olfactory neurons. Brain Res 103:555–559

    Google Scholar 

  • Døving KB (1964) Studies of the relation between the frog's electro-olfactogram (EOG) and single unit activity in the olfactory bulb. Acta Physiol Scand 60:150–163

    Google Scholar 

  • Døving KB (1987) Response properties of neurons in the rat olfactory bulb to various parameters of odour stimulation. Acta Physiol Scand 130:285–298

    Google Scholar 

  • Døving KB, Selset R, Thommesen G (1980) Olfactory sensitivity to bile acids in salmonid fishes. Acta Physiol Scand 108:123–131

    Google Scholar 

  • Duncan HJ, Nickell WT, Shipley MT, Gesteland RC (1990) Organization of projections from olfactory epithelium to olfactory bulb in the frog, Rana pipiens. J Comp Neurol 299:299–311

    Google Scholar 

  • Edwards DA, Mather RA, Dodd GH (1988) Spatial variation in response to odorants on the rat olfactory epithelium. Experientia 44:208–211

    Google Scholar 

  • Freeman WJ (1978) Spatial properties of an EEG event in the olfactory bulb and cortex. Electroencephalogr Clin Neurophysiol 44:586–605

    Google Scholar 

  • Green JD, Mancia M, Yrarrazaval S (1963) The role of mechanical factors in the responses of single olfactory bulb neurons. Acta Physiol Latinoam 13:347–349

    Google Scholar 

  • Guthrie KM, Anderson AJ, Leon M, Gall C (1993) Odor-induced increases in c-fos mRNA expression reveal an anatomical “unit” for odor processing in olfactory bulb. Proc Natl Acad Sci USA 90:3329–3333

    Google Scholar 

  • Hamilton KA, Kauer JS (1989) Patterns of intracellular potentials in salamander mitral/tufted cells in response to odor stimulation. J Neurophysiol 62:609–625

    Google Scholar 

  • Harrison TA, Scott JW (1986) Olfactory bulb responses to odor stimulation: analysis of response pattern and intensity relationships. J Neurophysiol 56:1571–1589

    Google Scholar 

  • Imamura K, Magata N, Mori K (1992) Coding of odor molecules by mitral/tufted cells in rabbit olfactory bulb. I. Aliphatic compounds. J Neurophysiol 68:1986–2002

    Google Scholar 

  • Jastreboff PJ, Pedersen PE, Greer CA, Steward WB, Kauer JS, Benson TE, Shepherd GM (1984) Specific olfactory receptor populations projecting to identified glomeruli in the rat olfactory bulb. Proc Natl Acad Sci USA 81:5250–5254

    Google Scholar 

  • Jiang T, Holley A (1992) Some properties of receptive fields of olfactory mitral/tufted cells in the frog. J Neurophysiol 68:726–733

    Google Scholar 

  • Jourdan F, Duveau A, Astic L, Holley A (1980) Spatial distribution of [14C]2-deoxyglucose uptake in the olfactory bulbs of rats stimulated with two different odours. Brain Res 188:139–154

    Google Scholar 

  • Kato K, Koshimoto H, Tani A, Mori K (1993) Coding of odor molecules by mitral/tufted cells in rabbit olfactory bulb. II. Aromatic compounds. J Neurophysiol 70:2161–2175

    Google Scholar 

  • Kauer JS (1974) Response patterns of amphibian olfactory bulb neurones to odour stimulation. J Physiol (Lond) 243:695–715

    Google Scholar 

  • Kauer JS (1981) Olfactory receptor cell staining using horseradish peroxidase. Anat Rec 200:331–336

    Google Scholar 

  • Kauer JS, Moulton DG (1974) Responses of olfactory bulb neurones to odour stimulation of small nasal areas in the salamander. J Physiol (Lond) 243:717–737

    Google Scholar 

  • Kauer JS, Senseman DM, Cohen LB (1987) Odor-elicited activity monitored simultaneously from 124 regions of the salamander olfactory bulb using a voltage-sensitive dye. Brain Res 418:255–261

    Google Scholar 

  • Kent PF, Mozell MM (1992) The recording of odorant-induced mucosal activity patterns with a voltage-sensitive dye. J Neurophysiol 68:1804–1819

    Google Scholar 

  • Key B, Akeson RA (1993) Distinct subsets of sensory olfactory neurons in mouse: possible role in the formation of the mosaic olfactory projection. J Comp Neurol 335:355–368

    Google Scholar 

  • Land LJ (1973) Localized projection of olfactory nerves to rabbit olfactory bulb. Brain Res 63:153–166

    Google Scholar 

  • Land LJ, Shepherd GM (1974) Autoradiographic analysis of olfactory receptor projections in the rabbit. Brain Res 70:506–510

    Google Scholar 

  • Lu X-C M, Slotnick BM (1994) Recognition of propionic acid vapor after removal of the olfactory bulb area associated with high 2-DG uptake. Brain Res 639:26–32

    Google Scholar 

  • Mackay-Sim A, Kesteven S (1994) Topographic patterns of responsiveness to odorants in the rat olfactory epithelium. J Neurophysiol 71:150–160

    Google Scholar 

  • Mackay-Sim A, Shaman P, Moulton DG (1982) Topographic coding of olfactory quality: odorant-specific patterns of epithelial responsivity in the salamander. J Neurophysiol 48:584–596

    Google Scholar 

  • Macleod NK (1976) Spontaneous activity of single neurons in the olfactory bulb of the rainbow trout (Salmo gairdneri) and its modulation by olfactory stimulation with amino acids. Exp Brain Res 25:267–278

    Google Scholar 

  • Macrides F, Chorover SL (1972) Olfactory bulb units: activity correlated with inhalation cycles and odor quality. Science 175:84–87

    Google Scholar 

  • Mathews DF (1972a) Response patterns of single neurons in the tortoise olfactory epithelium and olfactory bulb. J Gen Physiol 60:166–180

    Google Scholar 

  • Mathews DF (1972b) Response patterns of single units in the olfactory bulb of the rat to odor. Brain Res 47:389–400

    Google Scholar 

  • McBride SA, Slotnick BM, Graham SJ, Graziadei PPC (1985) Failure to find specific anosmias in rats with olfactory bulb lesions (abstract). Chem Senses 10:410

    Google Scholar 

  • Meredith M (1986) Patterned response to odor in mammalian olfactory bulb: the influence of intensity. J Neurophysiol 56:572–597

    Google Scholar 

  • Meredith M, Moulton DG (1978) Patterned response to odor in single neurons of goldfish olfactory bulb: influence of odor quality and other stimulus parameters. J Gen Physiol 71:615–643

    Google Scholar 

  • Motokizawa F, Ogawa Y (1987) Well controlled odor stimulation. Nippon Seirigaku Zasshi 49:701–710

    Google Scholar 

  • Motokizawa F, Ogawa Y (1990) Mechanosensitivity and its interference with chemosensitivity of an olfactory bulb neuron in the cat (abstract). In: Døving KB (ed) ISOT X. GCS AS, Oslo, p 341

    Google Scholar 

  • Motokizawa F, Ogawa Y (1992) Bursting: a basic property of olfactory bulb cell discharge (abstract). Chem Senses 17:865

    Google Scholar 

  • Mozell MM, Jagodowicz M (1973) Chromatographic separation of odorants by the nose: retention times measured across in vivo olfactory mucosa. Science 181:1247–1249

    Google Scholar 

  • Mustaparta H (1971) Spatial distribution of receptor responses to stimulation with different odours. Acta Physiol Scand 82:154–166

    Google Scholar 

  • Nickell WT, Shipley MY (1992) Neurophysiology of the olfactory bulb. In: Serby MJ, Chobor KL (eds) Science of olfaction. Springer, Berlin Heidelberg New York, pp 172–212

    Google Scholar 

  • Pagano RR (1966) The effects of central stimulation and nasal air flow on induced activity of olfactory structures. Electroencephalogr Clin Neurophysiol 21:269–277

    Google Scholar 

  • Reinken U, Schmidt U (1986) Reactions of olfactory bulb neurons to different intensities in laboratory mice. Exp Brain Res 63:151–157

    Google Scholar 

  • Ressler KJ, Sullivan SL, Buch LB (1993) A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 73:597–609

    Google Scholar 

  • Ressler KJ, Sullivan SL, Buch LB (1994) Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 79:1245–1255

    Google Scholar 

  • Saucier D, Astic L (1986) Analysis of the topographical organization of olfactory epithelium projections in the rat. Brain Res Bull 16:455–462

    Google Scholar 

  • Skeen LC (1977) Odor-induced patterns of deoxyglucose consumption in the olfactory bulb of the tree shrew, Tupaia glis. Brain Res 124:147–153

    Google Scholar 

  • Sklar PB, Anholt RH, Snyder SH (1986) The odorant-sensitive adenylate cyclase of olfactory receptor cells. J Biol Chem 261:15538–15543

    Google Scholar 

  • Stewart WB, Pedersen PE (1987) The spatial organization of olfactory nerve projections. Brain Res 411:248–258

    Google Scholar 

  • Stewart WB, Kauer JS, Shepherd GM (1979) Functional organization of rat olfactory bulb analyzed by the 2-deoxyglucose method. J Comp Neurol 185:715–734

    Google Scholar 

  • Tanabe T, Iino M, Takagi SF (1975) Discrimination of odors in olfactory bulb, pyriform-amygdaloid areas, and orbitofrontal cortex of the monkey. J Neurophysiol 38:1284–1296

    Google Scholar 

  • Thommesen G (1978) The distribution of odour induced potentials in the olfactory bulb of char and trout (Salmonidae). Acta Physiol Scand 102:205–217

    Google Scholar 

  • Thommesen G, Døving KB (1977) Spatial distribution of the EOG in the rat; a variation with odour quality. Acta Physiol Scand 99:270–280

    Google Scholar 

  • Ueki S, Domino EF (1961) Some evidence for a mechanical receptor in olfactory function. J Neurophysiol 24:12–25

    Google Scholar 

  • Vassar R, Ngai J, Axel R (1993) Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell 74:309–318

    Google Scholar 

  • Vassar R, Chao SK, Sitcheran R, Nunez JM, Vosshall LB, Axel R (1994) Topographic organization of sensory projections to the olfactory bulb. Cell 79:981–991

    Google Scholar 

  • Walsh RR (1956) Single spike activity in the olfactory bulb. Am J Physiol 186:255–257

    Google Scholar 

  • Wellis DP, Scott JW, Harrison TA (1989) Discrimination among odorants by single neurons of the rat olfactory bulb. J Neurophysiol 61:1161–1177

    Google Scholar 

  • Westecker ME (1970) Responses of single cells in the olfactory bulb of rabbits to air flow. Pflugers Arch 315:93–104

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Physiology, Nara Medical college, Kashihara, 634, Nara, Japan

    Fumiaki Motokizawa

Authors
  1. Fumiaki Motokizawa
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Motokizawa, F. Odor representation and discrimination in mitral/tufted cells of the rat olfactory bulb. Exp Brain Res 112, 24–34 (1996). https://doi.org/10.1007/BF00227174

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00227174

Key words

Search

Navigation