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Odor- and context-dependent modulation of mitral cell activity in behaving rats

Abstract

The projections and odor responses of mammalian olfactory receptor neurons, as well as the physiology of the bulb's principal neurons—the mitral cells (MCs)—are known from studies in slices and anesthetized animals. In behaving rats trained to discriminate between two odors associated with different reinforcers, we examined MC responses following alternated odor–reinforcer pairings. Whereas only 11% of the recorded MCs showed changes in odor-selective firing rate during the odor-sampling phase, 94% of MCs modulated activity during specific behaviors surrounding odor sampling. These cell- and odor-selective responses were not primary sensory responses; rather, they depended (reversibly) on the predictive value of each odor. MC activity thus depends critically on efferent influences linked to the animal's experience and behavior.

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Figure 1: Behavioral paradigm, mitral cell unit isolation and experimental design.
Figure 2: Identification of recording sites in the OB using a 16-channel silicon probe.
Figure 3: Respiratory driving of single units.
Figure 4: Behavioral modulation of firing rate.
Figure 5: Behavior-associated modulations in firing rate for three cells recorded simultaneously from three different electrodes.
Figure 6: Odor-selective differences in firing rate during odor identification.

References

  1. Buonviso, N. & Chaput, M. A. 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 (1990).

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  3. Mori, K., Mataga, N. & Imamura, K. Differential specificities of single mitral cells in rabbit olfactory bulb for a homologous series of fatty acid odor molecules. J. Neurophysiol. 67, 786– 789 (1992).

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  5. Motokizawa, F. Odor representation and discrimination in mitral tufted cells of the rat olfactory bulb. Exp. Brain Res. 112, 24– 34 (1996).

    CAS  Article  Google Scholar 

  6. Viana di Prisco, G. & Freeman, W. J. Odor-related bulbar EEG spatial pattern analysis during appetitive conditioning in rabbits. Behav. Neurosci. 99, 964– 978 (1985).

    Article  Google Scholar 

  7. de Olmos, J., Hardy, H. & Heimer, L. The afferent connections of the main and the accessory olfactory bulb formations in the rat: an experimental HRP-study. J. Comp. Neurol. 181, 213–244 (1978).

    CAS  Article  Google Scholar 

  8. Shipley, M. T. & Adamek, G. D. The connections of the mouse olfactory bulb: a study using orthograde and retrograde transport of wheat germ agglutinin conjugated to horseradish peroxidase. Brain Res. Bull. 12, 669–688 (1984).

    CAS  Article  Google Scholar 

  9. van Groen, T. & Wyss, J. M. Extrinsic projections from area CA1 of the rat hippocampus: olfactory, cortical, subcortical, and bilateral hippocampal formation projections. J. Comp. Neurol. 302, 515–528 ( 1990).

    CAS  Article  Google Scholar 

  10. Carmichael, S. T., Clugnet, M. C. & Price, J. L. Central olfactory connections in the macaque monkey. J. Comp. Neurol. 346, 403– 434 (1994).

    CAS  Article  Google Scholar 

  11. Jansen, H. T., Iwamoto, G. A. & Jackson, G. L. Central connections of the ovine olfactory bulb formation identified using wheat germ agglutinin-conjugated horseradish peroxidase. Brain Res. Bull. 45, 27– 39 (1998).

    CAS  Article  Google Scholar 

  12. Pager, J. Unit responses changing with behavioral outcome in the olfactory bulb of unrestrained rats. Brain Res. 289, 87– 98 (1983).

    CAS  Article  Google Scholar 

  13. Chaput, M. A. & Holley, A. Responses of olfactory bulb neurons to repeated odor stimulations in awake freely-breathing rabbits. Physiol. Behav. 34, 249–258 (1985).

    CAS  Article  Google Scholar 

  14. Pager, J. Respiration and olfactory bulb unit activity in the unrestrained rat: statements and reappraisals. Behav. Brain Res. 16, 81–94 (1985).

    CAS  Article  Google Scholar 

  15. Bhalla, U. S. & Bower, J. M. Multiday recordings from olfactory bulb neurons in awake freely moving rats: spatially and temporally organized variability in odorant response properties. J. Comput. Neurosci. 4, 221–256 ( 1997).

    CAS  Article  Google Scholar 

  16. Wehr, M. & Laurent, G. Odour encoding by temporal sequences of firing in oscillating neural assemblies. Nature 384, 162–166 (1996).

    CAS  Article  Google Scholar 

  17. Darling, F. M. & Slotnick, B. M. Odor-cued taste avoidance: a simple and efficient method for assessing olfactory detection, discrimination and memory in the rat. Physiol. Behav. 55, 817–822 (1994).

    CAS  Article  Google Scholar 

  18. Paxinos, G. & Watson, C. The Rat Brain in Stereotaxic Coordinates (Academic, New York, 1986).

    Google Scholar 

  19. Bragin, A. et al. Gamma (40–100 Hz) oscillation in the hippocampus of the behaving rat. J. Neurosci. 15, 47– 60 (1995).

    CAS  Article  Google Scholar 

  20. Sobel, E. C. & Tank, D. W. Timing of odor stimulation does not alter patterning of olfactory bulb unit activity in freely breathing rats. J. Neurophys. 69, 1331– 1337 (1993).

    CAS  Article  Google Scholar 

  21. Gray, C. M. & Skinner, J. E. Centrifugal regulation of neuronal activity in the olfactory bulb of the waking rabbit as revealed by reversible cryogenic blockade. Exp. Brain Res. 69, 378–386 (1988).

    CAS  Article  Google Scholar 

  22. Kay, L. M. & Freeman, W. J. Bidirectional processing in the olfactory-limbic axis during olfactory behavior. Behav. Neurosci. 112, 541–553 ( 1998).

    CAS  Article  Google Scholar 

  23. Rhinehart-Doty, J. A., Schumm, J., Smith, J. C. & Smith, G. P. A non-taste cue of sucrose in short-term taste tests in rats. Chem. Senses 19, 425–431 (1994).

    CAS  Article  Google Scholar 

  24. Miller, S. D. & Erickson, R. P. The odor of taste solutions. Physiol. Behav. 1, 145– 146 (1966).

    Article  Google Scholar 

  25. Stewart, W. B., Kauer, J. S. & Shepherd, G. M. Functional organization of rat olfactory bulb analysed by the 2- deoxyglucose method. J. Comp. Neurol. 185 , 715–734 (1979).

    CAS  Article  Google Scholar 

  26. Johnson, B. A., Woo, C. C. & Leon, M. Spatial coding of odorant features in the glomerular layer of the rat olfactory bulb. J. Comp. Neurol. 393, 457–471 (1998).

    CAS  Article  Google Scholar 

  27. Schoenbaum, G., Chiba, A. A. & Gallagher, M. Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning. Nat. Neurosci. 1 , 155–159 (1998).

    CAS  Article  Google Scholar 

  28. Schoenbaum, G., Chiba, A. A. & Gallagher, M. Neural encoding in orbitofrontal cortex and basolateral amygdala during olfactory discrimination learning. J. Neurosci. 19, 1876–1884 ( 1999).

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  30. Freeman, W. J., Viana Di Prisco, G., Davis, G. W. & Whitney, T. M. Conditioning of relative frequency of sniffing by rabbits to odors. J. Comp. Psychol. 97, 12–23 (1983).

    CAS  Article  Google Scholar 

  31. Gray, C. M. & Skinner, J. E. Field potential response changes in the rabbit olfactory bulb accompany behavioral habituation during the repeated presentation of unreinforced odors. Exp. Brain Res. 73, 189–197 (1988).

    CAS  Article  Google Scholar 

  32. Dave, A. S., Yu, A. C. & Margoliash, D. Behavioral state modulation of auditory activity in a vocal motor system. Science 282, 2250– 2254 (1998).

    CAS  Article  Google Scholar 

  33. Schmidt, M. F. & Konishi, M. Gating of auditory responses in the vocal control system of awake songbirds. Nat. Neurosci. 1, 513–518 ( 1998).

    CAS  Article  Google Scholar 

  34. Klingberg, F. & Pickenhain, L. Über langsame atemsynchrone Potentiale vom Bulbus olfactorius der Ratte. Acta Biol. Med. Ger. 14, 593–595 ( 1965).

    CAS  PubMed  Google Scholar 

  35. Kay, L. M., Lancaster, L. R. & Freeman, W. J. Reafference and attractors in the olfactory system during odor recognition. Int. J. Neural Syst. 7, 489–495 (1996).

    CAS  Article  Google Scholar 

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Acknowledgements

We are grateful to Steven Notari, Vali Mohammadi, Lindsey Drake and Maryellen Begley for assistance with surgery, electronics, histology and animal handling, to Lucia Jacobs for the loan of behavioral equipment (NSF grant IBN-9307317), to Mark Stopfer and Brian Smith for statistical advice, to Christophe Pouzat for assistance with the silicon probe recordings and to Erin Schuman, Rainer Friedrich and Mark Stopfer for comments on the manuscript. Silicon probes were obtained from the University of Michigan Center for Neural Communication Technology (NIH/NCRR grant P41-RR09754). Supported by grants from the Sloan Center for Theoretical Neuroscience at Caltech, the Keck Foundation, the Burroughs-Wellcome Center for Computational Molecular Biology at Caltech, the NSF and the NIDCD.

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Correspondence to Gilles Laurent.

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Kay, L., Laurent, G. Odor- and context-dependent modulation of mitral cell activity in behaving rats. Nat Neurosci 2, 1003–1009 (1999). https://doi.org/10.1038/14801

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