Journal of Computational Neuroscience

, Volume 4, Issue 3, pp 221–256 | Cite as

Multiday Recordings from Olfactory Bulb Neurons in Awake Freely Moving Rats: Spatially and Temporally Organized Variability in Odorant Response Properties

  • Upinder S. Bhalla
  • James M. Bower


Chronic single-unit recordings were obtained from the mitral celllayer of the olfactory bulbs of awake freely moving rats placed in anodorant stream. Over periods up to five days, 618 recordings from 186single neurons were obtained. Responses of individual neurons werefound to be quite variable over time, although this variability wasbelow chance and was not incremental. The responses of nearbyneurons were more similar than expected by chance but less similarthan individual neurons recorded at different times. However,responses of spatially well-separated neurons were more differentthan chance over short time periods. During rapid sniffing,single-unit responses became more variable, and the spatialorganization of responses became less apparent. These results suggestthat neuronal responses in the olfactory bulb are generally quitevariable over time, with this variability increasing during periodsof rapid sniffing. These results are interpreted in the context of adistributed, centrally modulated model of olfactoryprocessing.

olfaction olfactory bulb mitral/tufted cell stereo electrode multiday recording chronic implant awake behaving distributed representation 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alberts JR, Galef BG, Jr. (1971) Acute anosmia in the rat: A behavioral test of a peripherally induced olfactory deficit. Physiol. Behav.6:619–621.Google Scholar
  2. Arieli A, Sterkin A, Grinvald A, Aertsen A (1996) Dynamics of ongoing activity: Explanation of the large variability in evoked cortical responses. Science273:1868–1871.Google Scholar
  3. Astic L, Saucier D, Holley A (1987) Topgraphical relationships between olfactory receptor cells and glomerular foci in the rat olfactory bulb. Brain Res.424:144–152.Google Scholar
  4. Baldi P, Heiligenberg W (1988) How sensory maps could enhance resolution through ordered arrangments of broadly tuned receivers. Biol. Cybern.59:313–318.Google Scholar
  5. Bhalla US, Bower JM (1993) Exploring parameter space in detailed single neuron models: Simulations of the mitral and granule cells of the olfactory bulb. J. Neurophysiol.69(6):1948–1965.Google Scholar
  6. Bialek W, Rieke F (1992) Reliability and information transmission in spiking neurons. Trends Neurosci.15(11):428–434.Google Scholar
  7. Bower JM (1995) Reverse engineering the nervous system: An in vivo, in vitro, and in computoapproach to understanding the mammalian olfactory system. 2nd edition. In: S Zornetzer, J Davis, C Lau, eds. An Introduction to Neural and Electronic Networks, Academic Press, New York. pp. 3–28.Google Scholar
  8. Buck L (1996) Information coding in the vertebrate olfactory system. Annu. Rev. Neurosci.19:517–544.Google Scholar
  9. Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: A molecular basis for odor recognition. Cell65:175–187.Google Scholar
  10. Buonviso N, Chaput MA (1990) Response similarity to odors in olfactory bulb output cells presumed to be connected to the same glomerulus: Electrophysiological study using simultaneous single-unit recordings. J. Neurophysiol.63:447–454.Google Scholar
  11. Buonviso N, Chaput MA, Berthommier F (1992) Temporal pattern analyses in pairs of neighboring mitral cells. J. Neurophysiol. 68:417–424.Google Scholar
  12. Chaput MA (1986) Respiratory-phase-related coding of olfactory information in the olfactory bulb of awake freely-breathing rabbits. Physiology and Behavior36:319–324.Google Scholar
  13. Chaput MA, Holley A (1979) Spontaneous activity of olfactory bulb neurons in awake rabbits with some observations on the effects of pentobarbitol anesthesia. J. Physiol. Paris75:939–948.Google Scholar
  14. Chaput MA, Holley A (1985) Responses of olfactory bulb neurons to repeated odor stimulations in awake freely-breathing rabbits. Physiol. and Behav.34:249–258.Google Scholar
  15. Chaput MA, Lankheet MJ (1987) Influence of stimulus intensity on the categories of single-unit responses recorded from olfactory bulb neurons in awake freely breathing rabbits. Physiology and Behavior40:453–462.Google Scholar
  16. Chaput MA, Buonviso N, Berthommie F (1992) Temporal patterns in spontaneous and odour-evoked mitral cell discharges recorded in anaesthetized freely breathing animals. Eur. J. Neuroscience 4:813–822.Google Scholar
  17. Chess A, Simon I, Cedar H, Axel R (1994) Allelic inactivation regulates olfactory receptor gene expression. Cell78:823–834.Google Scholar
  18. 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(5):2053–2071.Google Scholar
  19. Cinelli AR, Salzberg BM(1992) Dendritic origin of late events in optical recordings from salamander olfactory bulb. J. Neurophysiol. 68:786–806.Google Scholar
  20. Devor M (1976). Fiber trajectories of olfactory bulb efferents in the hamster. J. Comp. Neurol.166:31–48.Google Scholar
  21. Dickinson TA, White J, Kauer JS, Walt DR (1996) A chemical detercting system based on a cross-reactive optical sensory array. Nature382:697–700.Google Scholar
  22. Duchamp-Viret P, Duchamp A, Sicard G (1990) Olfactory discrimination over a wide concentration range: Comparison of receptor cell and bulb neuron properties. Brain Res.517:256–262.Google Scholar
  23. Freeman WJ (1991) The physiology of perception. Scientific American 264(2):78–85.Google Scholar
  24. Fujita SC, Mori KR, Imamura D, Obata K (1985) Subclasses of olfactory receptor cells and their segregated central projections demonstrated by a monclonal antibody. Brain Res.326:192–196.Google Scholar
  25. Furster D, Spruston N (1995) Cracking the neuronal code. Science 270:756–757.Google Scholar
  26. Gerstein GL, Aertsen AMHJ (1985) Representation of cooperative firing among simultaneously recorded neurons. J. Neurophys. 54:1513–1528.Google Scholar
  27. Goldberg SJ, Moulton DG (1987) Olfactory bulb responses telemetered during an odor discrimination task in rats. Exp. Neurology 96:430–442.Google Scholar
  28. Granger R, Ambros-Ingerson J, Lynch G (1988) Derivation of encoding characteristics of layer II cerebral cortex. J. Cogn. Neurosci. 1:64–91.Google Scholar
  29. Gray CM, Skinner JE (1988) Centrifugal regulation of neuronal activity in the olfactory bulb of the waking rabbit as revealed by cryogenic blockade. Exp. Brain Res.69:378–386.Google Scholar
  30. Graziadei PPC, Monti Graziadei GA (1979) Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neurons. J. Neurocytol.8:1–18.Google Scholar
  31. Haberly LB (1985). Neuronal circuitry in olfactory cortex: Anatomy and functional implications. Chemical Senses10:219–238.Google Scholar
  32. Hamilton KA, Kauer JS (1985) Intracellular potentials of salamander mitral/tufted neurons in response to odor stimulation. Brain Res. 338:181–118.Google Scholar
  33. 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
  34. Hasselmo ME, Bower JM (1993) Acetylcholine and memory. Trends in Neurosci.16:218–222.Google Scholar
  35. Holley A Sicard G (1984) Receptor cell responses to odorants: Similarities and differences among odorants. Brain Res.292:283–296.Google Scholar
  36. Imamura K, Mataga 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
  37. 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
  38. Jourdan F, Duveau A, Astic L, Holley A (1980) Spatial distribution of 2-deoxyglucose uptake in the olfactory bulbs of rats stimulated with two different odors. Brain Res.188:139–154.Google Scholar
  39. Katoh 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
  40. Kauer JS (1974) Response properties of amphibian olfactory bulb neurones to odour stimulation. J. Physiol. Lond.243:695–715.Google Scholar
  41. Kauer JS (1987) Coding in the Olfactory System. In: TE Finger, WL Silver, eds. Neurobiology of Taste and Smell. Wiley, New York.Google Scholar
  42. Kauer JS (1988) Real-time imaging of evoked activity in local circuits of the salamander olfactory bulb. Nature331:166–168.Google Scholar
  43. Kauer JS, Shepherd GM (1977) Analysis of the onset phase of olfactory bulb unit responses to odour pulses in the salamander. J. Physiol. Lond.272:495–516.Google Scholar
  44. Keppel G (1982) Design and Analysis: A Researcher’s Handbook. 2nd edition. Prentice-Hall, New Jersey.Google Scholar
  45. Kurahashi T, Lowe G, Gold GH (1994) Suppression of odorant responses by odorants in olfactory receptor cells. Science265:118–120.Google Scholar
  46. Lancet D (1986) Vertebrate olfactory reception. Ann. Rev. Neurosci. 9:329–355.Google Scholar
  47. Lancet D, Greer CA, Kauer JS, Shepherd GM (1982) Mapping of odor-related neuronal activity in the olfactory bulb by highresolution 2-deoxyglucose autoradiography Proc. Natl. Acad. Sci. 79:670–674.Google Scholar
  48. Laurent G (1996) Odor images and tunes. Neuron16:473–476.Google Scholar
  49. Laurent G, Davidowitz H (1994) Encoding of olfactory information with oscillating neural assemblies. Science265:1872–1875.Google Scholar
  50. Lonergan MC, Severin EJ, Doleman BJ, Grubb RH, Lewis N (1996) Array-based vapor sensing using chemically sensitive carbon black-polymer resistors. Chem-mater88:2298–2312.Google Scholar
  51. Macrides F, Chorover SL(1972) Olfactory bulb units: Activity correlated with inhalation cycles and odor quality. Science175:84–87.Google Scholar
  52. Mainen ZF, Sejnowski TJ (1995) Reliability of spike timing in neocortical neurons. Science268:1503–1506.Google Scholar
  53. Mair RG (1982) Response properties of olfactory bulb neurons. J. Physiol. Lond.326:341–359.Google Scholar
  54. McNaughton BL, O’Keefe J, Barnes CA (1983) The stereotrode: A new technique for simultaneous isolation of several single units in the central nervous system from multiple unit records. J. Neurosci. Meth.8:391–397.Google Scholar
  55. Meredith M (1986) Patterned response to odor in mammalian olfactory bulb: The influence of intensity. J. Neurophysiol.56:572–597.Google Scholar
  56. Meredith M (1992) Sensory processing in the main and accessory olfactory systems: Comparisons and contrasts. J. Steroid Biochem. Molec. Biol.39(4B):601–614,(1991) 29:111–117.Google Scholar
  57. Mori K (1987) Membrane and synaptic properties of identified neurons in the olfactory bulb. Progress in Neurobio.29:275–320.Google Scholar
  58. Mori K, Mataga N, Imamura K (1992) Differential specificities of single mitral cells in rabbit olfactory bulb from a homologous series of fatty acid odor molecules. J. Neurophysiol.67:786–789.Google Scholar
  59. Nicolelis MAL, Baccala LA, Lin RCS, Chapin JK (1995) Sensorimotor encoding by synchronous neural ensemble activity at multiple levels of the somatosensory system. Science268:1353–1358.Google Scholar
  60. Pager J (1985) Respiration and olfactory bulb unit activity in the unrestrained rat: Statements and reappraisals. Behav. Brain Res. 16:81–94.Google Scholar
  61. Press WH, Flannery BP, Teukolsky SA, Vetterling WT (1988) The Art of Scientific Computing. Cambridge University Press, Cambridge.Google Scholar
  62. Rall W, Shepherd GM (1968) Theoretical reconstruction of field potentials and dendrodendritic synaptic interactions in olfactory bulb. J. Neurophysiol.31:884–915.Google Scholar
  63. Rawson NE, Restrepo D (1995) Does a single olfactory neuron express one or more receptor genes? Soc. Neurosci. Abst.21:131.Google Scholar
  64. Ressler KJ, Sullivan SL, Buck LB (1993) A Zonal Organization of odorant receptor gene expression in the olfactory epithelium. Cell 79:1245–1256.Google Scholar
  65. Rumelhart DE, McClelland JL (1986) Parallel Distributed Processing. MIT Press, Cambridge, MA.Google Scholar
  66. Scott JW (1977) Ameasure of extracellular unit responses to repeated stimulation applied to observations of the time course of olfactory responses. Brain Res.132:247–258.Google Scholar
  67. Shadlen MN, Newsome WT (1994) Noise, neural codes and cortical organization. Curr Opinion Neurobiol. 4:569–579.Google Scholar
  68. Shepherd GM (1993) Principles of specificity and redundancy underlying the organization of the olfactory system. Microscopy Research and Technique24:106–112.Google Scholar
  69. Sicard G, Holley A (1984) Receptor cell responses to odorants: Similarities and differences among odorants. Brain Res.292:283–296.Google Scholar
  70. Slotnick BM, Nigrosh BJ (1974) Olfactory stimulus control evaluated in a small animal olfactometer. Perceptual and Motor Skills 39:583–597.Google Scholar
  71. Slotnick BM, Graham S, Laing DG, Bell GA (1987) Detection of propionic acid vapor by rats with lesions of olfactory bulb areas associated with high 2-DG uptake. Brain Res.417:343–346.Google Scholar
  72. Slotnick BM, Kufera A, Silberberg AM (1991)Olfactory learning and odor memory in the rat. Physiol. and Behav.50:555–561.Google Scholar
  73. Snedecor GW, Cochran WG (1967) Statistical Methods. 6th edition. Iowa State University Press, Ames.Google Scholar
  74. Softky WR, Koch C (1993) The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J. Neurosci.13(1):334–350.Google Scholar
  75. Stewart WB, Kauer JS, Shepherd GM (1979) Functional organization of rat olfactory bulb analyzed by the 2-deoxyglucose method. J. Comp. Neurol.185(4):715–734.Google Scholar
  76. 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
  77. 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
  78. Wilson DA, Leon M (1987) Evidence of lateral synaptic interactions in olfactory bulb output cell responses to odors. Brain Res. 417:175–180.Google Scholar
  79. Youngentob SL, Mozell MM, Sheehe PR, Hornung DE (1987) A quantitative analysis of sniffing strategies in rats performing odor detection tasks. Physiol. and Behav.41:59–69.Google Scholar

Copyright information

© Kluwer Academic Publishers 1997

Authors and Affiliations

  • Upinder S. Bhalla
    • 1
    • 2
  • James M. Bower
    • 3
  1. 1.Division of BiologyCalifornia Institute of TechnologyPasadena
  2. 2.National Centre for Biological Sciences, TIFR Centre, IISc CampusBangaloreIndia
  3. 3.Division of BiologyCalifornia Institute of TechnologyPasadena

Personalised recommendations