Synchronized oscillatory discharges of mitral/tufted cells with different molecular receptive ranges in the rabbit olfactory bulb.

Individual glomeruli in the mammalian olfactory bulb represent a single or a few type(s) of odorant receptors. Signals from different types of receptors are thus sorted out into different glomeruli. How does the neuronal circuit in the olfactory bulb contribute to the combination and integration of signals received by different glomeruli? Here we examined electrophysiologically whether there were functional interactions between mitral/tufted cells associated with different glomeruli in the rabbit olfactory bulb. First, we made simultaneous recordings of extracellular single-unit spike responses of mitral/tufted cells and oscillatory local field potentials in the dorsomedial fatty acid-responsive region of the olfactory bulb in urethan-anesthetized rabbits. Using periodic artificial inhalation, the olfactory epithelium was stimulated with a homologous series of n-fatty acids or n-aliphatic aldehydes. The odor-evoked spike discharges of mitral/tufted cells tended to phase-lock to the oscillatory local field potential, suggesting that spike discharges of many cells occur synchronously during odor stimulation. We then made simultaneous recordings of spike discharges from pairs of mitral/tufted cells located 300-500 microm apart and performed a cross-correlation analysis of their spike responses to odor stimulation. In approximately 27% of cell pairs examined, two cells with distinct molecular receptive ranges showed synchronized oscillatory discharges when olfactory epithelium was stimulated with one or a mixture of odorant(s) effective in activating both. The results suggest that the neuronal circuit in the olfactory bulb causes synchronized spike discharges of specific pairs of mitral/tufted cells associated with different glomeruli and the synchronization of odor-evoked spike discharges may contribute to the temporal binding of signals derived from different types of odorant receptor.

[1]  Richard Axel,et al.  Visualizing an Olfactory Sensory Map , 1996, Cell.

[2]  Gordon M. Shepherd,et al.  Discrimination of molecular signals by the olfactory receptor neuron , 1994, Neuron.

[3]  G. Laurent,et al.  Distinct Mechanisms for Synchronization and Temporal Patterning of Odor-Encoding Neural Assemblies , 1996, Science.

[4]  W. Singer,et al.  Stimulus‐Dependent Neuronal Oscillations in Cat Visual Cortex: Inter‐Columnar Interaction as Determined by Cross‐Correlation Analysis , 1990, The European journal of neuroscience.

[5]  G. Laurent,et al.  Odour encoding by temporal sequences of firing in oscillating neural assemblies , 1996, Nature.

[6]  H. Kaba,et al.  Synaptic Mechanisms of Olfactory Recognition Memory , 1995, Reviews in the neurosciences.

[7]  K. Mori,et al.  Coding of odor molecules by mitral/tufted cells in rabbit olfactory bulb. II. Aromatic compounds. , 1992, Journal of neurophysiology.

[8]  Gordon M. Shepherd,et al.  The Olfactory Bulb , 1988 .

[9]  Richard Axel,et al.  Topographic organization of sensory projections to the olfactory bulb , 1994, Cell.

[10]  P. König.  A method for the quantification of synchrony and oscillatory properties of neuronal activity , 1994, Journal of Neuroscience Methods.

[11]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[12]  G. Shepherd,et al.  Functional organization of rat olfactory bulb analysed by the 2‐deoxyglucose method , 1979, The Journal of comparative neurology.

[13]  K. Imamura,et al.  Differential specificities of single mitral cells in rabbit olfactory bulb for a homologous series of fatty acid odor molecules. , 1992, Journal of neurophysiology.

[14]  K. Ressler,et al.  The chromosomal distribution of mouse odorant receptor genes. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[15]  J. Royet,et al.  Morphometric modifications associated with early sensory experience in the rat olfactory bulb: II. Stereological study of the population of olfactory glomeruli , 1989, The Journal of comparative neurology.

[16]  P. Mombaerts,et al.  Molecular biology of odorant receptors in vertebrates. , 1999, Annual review of neuroscience.

[17]  Yoshihiro Yoshihara,et al.  Molecular recognition and olfactory processing in the mammalian olfactory system , 1995, Progress in Neurobiology.

[18]  W. Freeman,et al.  Frequency analysis of olfactory system EEG in cat, rabbit, and rat. , 1980, Electroencephalography and clinical neurophysiology.

[19]  R. Axel,et al.  A novel multigene family may encode odorant receptors: A molecular basis for odor recognition , 1991, Cell.

[20]  G. Laurent.  Dynamical representation of odors by oscillating and evolving neural assemblies , 1996, Trends in Neurosciences.

[21]  Steven L. Bressler,et al.  Relation of olfactory bulb and cortex. I. Spatial variation of bulbocortical interdependence , 1987, Brain Research.

[22]  G. Shepherd,et al.  Theoretical reconstruction of field potentials and dendrodendritic synaptic interactions in olfactory bulb. , 1968, Journal of neurophysiology.

[23]  L. Buck,et al.  Combinatorial Receptor Codes for Odors , 1999, Cell.

[24]  E. Adrian,et al.  The electrical activity of the mammalian olfactory bulb. , 1950, Electroencephalography and clinical neurophysiology.

[25]  E. Fetz,et al.  Synchronization of neurons during local field potential oscillations in sensorimotor cortex of awake monkeys. , 1996, Journal of neurophysiology.

[26]  P. Brennan,et al.  NEURAL MECHANISMS OF MAMMALIAN OLFACTORY LEARNING , 1997, Progress in Neurobiology.

[27]  K Kishi,et al.  Distribution of dendrites of mitral, displaced mitral, tufted, and granule cells in the rabbit olfactory bulb , 1983, The Journal of comparative neurology.

[28]  Nathalie Buonviso,et al.  Mitral cell‐to‐glomerulus connectivity: An HRP study of the orientation of mitral cell apical dendrites , 1991, The Journal of comparative neurology.

[29]  K. Imamura,et al.  Coding of odor molecules by mitral/tufted cells in rabbit olfactory bulb. I. Aliphatic compounds. , 1992, Journal of neurophysiology.

[30]  G M Shepherd,et al.  Dendrodendritic synaptic pathway for inhibition in the olfactory bulb. , 1966, Experimental neurology.

[31]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[32]  A. C. Allison,et al.  Quantitative observations on the olfactory system of the rabbit. , 1949, Brain : a journal of neurology.

[33]  Linda B. Buck,et al.  Information coding in the olfactory system: Evidence for a stereotyped and highly organized epitope map in the olfactory bulb , 1994, Cell.