Abstract
Information processing in the brain may rely on temporal correlations in spike activity between neurons. Within the olfactory bulb, correlated spiking in output mitral cells could affect the odor code by either binding or amplifying signals from individual odorant receptors. We examined the timing of spike trains in mitral cells of rat olfactory bulb slices. Depolarization of mitral cell pairs elicited spikes that were correlated on a rapid timescale (≤10 ms) for cells whose primary dendrites projected to the same glomerulus. Correlated spiking was driven by a novel mechanism that depended on electrical coupling at mitral cell primary dendrites; the specific synchronizing signal was a coupled depolarization (∼20 ms) that was mediated by dendritic AMPA autoreceptors. We suggest that glomerulus-specific correlated spiking in mitral cells helps to preserve the fidelity of odor signals that are delivered to the olfactory cortex.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Mori, K., Nagao, H. & Yoshihara, Y. The olfactory bulb: coding and processing of odor molecule information. Science 286, 711–715 (1999).
Bozza, T.C. & Mombaerts, P. Olfactory coding: revealing intrinsic representations of odors. Curr. Biol. 11, R687–R690 (2001).
Carr, C.E. Processing of temporal information in the brain. Annu. Rev. Neurosci. 16, 223–243 (1993).
Meister, M., Lagnado, L., & Baylor, D.A. Concerted signaling by retinal ganglion cells. Science 270, 1207–1210 (1995).
Laurent, G. et al. Odor encoding as an active, dynamical process: experiments, computation, and theory. Annu. Rev. Neurosci. 24, 263–297 (2001).
Friedrich, R.W. & Stopfer, M. Recent dynamics in olfactory population coding. Curr. Opin. Neurobiol. 11, 468–474 (2001).
Adrian, E.D. The electrical activity of the mammalian olfactory bulb. Electroencephalogr. Clin. Neurophysiol. 2, 377–388 (1950).
Freeman, W.J. Measurement of oscillatory responses to electrical stimulation in olfactory bulb of cat. J. Neurophysiol. 35, 762–779 (1972).
Kashiwadani, H., Sasaki, Y.F., Uchida, N. & Mori, K. Synchronized oscillatory discharges of mitral/tufted cells with different molecular receptive ranges in the rabbit olfactory bulb. J. Neurophysiol. 82, 1786–1792 (1999).
Stopfer, M., Bhagavan, S., Smith, B.H. & Laurent, G. Impaired odor discrimination on desynchronization of odor-encoding neural assemblies. Nature 390, 70–74 (1997).
Rall, W. & Shepherd, G.M. Theoretical reconstruction of field potentials and dendrodendritic synaptic interactions in the olfactory bulb. J. Neurophysiol. 31, 884–915 (1968).
Desmaisons, D., Vincent, J.D. & Lledo, P.M. Control of action potential timing by intrinsic subthreshold oscillations in olfactory bulb output neurons. J. Neurosci. 19, 10727–10737 (1999).
Nicoll, R.A. & Jahr, C.E. Self-excitation of olfactory bulb neurons. Nature 296, 441–444 (1982).
Aroniadou-Anderjaska, V., Ennis, M. & Shipley, M.T. Dendrodendritic recurrent excitation in mitral cells of the rat olfactory bulb. J. Neurophysiol. 82, 489–494 (1999).
Isaacson, J.S. Glutamate spillover mediates excitatory transmission in the rat olfactory bulb. Neuron 20, 377–384 (1999).
Friedman, D. & Strowbridge, B.W. Functional role of NMDA autoreceptors in olfactory mitral cells. J. Neurophysiol. 84, 39–50 (2000).
Salin, P.A., Lledo, P.M., Vincent, J.D. & Charpak, S. Dendritic glutamate autoreceptors modulate signal processing in rat mitral cells. J. Neurophysiol. 85, 1275–1282 (2001).
Paternostro, M.A., Reyher, C.K.H. & Brunjes, P.C. Intracellular injections of Lucifer yellow into lightly fixed mitral cells reveal neuronal dye-coupling in the developing rat olfactory bulb. Dev. Brain Res. 84, 1–10 (1995).
Miragall, F., Simburger, E. & Dermietzel, R. Mitral and tufted cells of the mouse olfactory bulb possess gap junctions and express connexin43 mRNA. Neurosci. Lett. 216, 199–202 (1996).
Belluardo, N. et al. Expression of connexin36 in the adult and developing rat brain. Brain Res. 865, 121–138 (2000).
Zhang, C. & Restrepo, D. Expression of connexin 45 in the olfactory system. Brain Res. 929, 37–47 (2002).
Schoppa, N.E. & Westbrook, G.L. Glomerulus-specific synchronization of mitral cells in the olfactory bulb. Neuron 31, 639–651 (2001).
Perez Velazquez, J.L. & Carlen, P.L. Gap junctions, synchrony and seizures. Trends Neurosci. 23, 68–74 (2000).
Gibson, J.R., Beierlein, M. & Connors, B.W. Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402, 75–79 (1999).
Venance, L. et al. Connexin expression in electrically coupled postnatal rat brain neurons. Proc. Natl. Acad. Sci. USA 97, 10260–10265 (2000).
Veenstra, R.D. Size and selectivity of gap junction channels formed from different connexins. J. Bioenerg. Biomembr. 28, 327–337 (1996).
Montague, A.A. & Greer, C.A. Differential distribution of ionotropic glutamate receptor subunits in the rat olfactory bulb. J. Comp. Neurol. 405, 233–246 (1999).
Dildy-Mayfield, J.E., Eger, E.I. & Harris, R.A. Anesthetics produce subunit-selective actions on glutamate receptors. J. Pharmacol. Exp. Ther. 276, 1058–1065 (1996).
Kirson, E.D., Yaari, Y. & Perouansky, M. Presynaptic and postsynaptic actions of halothane at glutamatergic synapses in the mouse hippocampus. Br. J. Pharmacol. 124, 1607–1614 (1998).
Williams, S.R. & Stuart, G.J. Dependence of EPSP efficacy on synapse location in neocortical pyramidal neurons. Science 295, 1907–1910 (2002).
Lei, H., Christensen, T.A. & Hildebrand, J.G. Local inhibition modulates odor-evoked synchronization of glomerulus-specific output neurons. Nat. Neurosci. 5, 557–565 (2002).
Carlson, G.C., Shipley, M.T. & Keller, A. Long-lasting depolarizations in mitral cells of the rat olfactory bulb. J. Neurosci. 20, 2011–2021 (2000).
Tamás, G., Buhl, E.H., Lorincz, A. & Somogyi, P. Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat. Neurosci. 3, 366–371 (2000).
Schmitz, D. et al. Axo-axonal coupling. A novel mechanism for ultrafast neuronal communication. Neuron 31, 831–840 (2001).
Brivanlou, I.H., Warland, D.K. & Meister, M. Mechanisms of concerted firing among retinal ganglion cells. Neuron 20, 527–539 (1998).
Teubner, B. et al. Functional expression of the murine connexin 36 gene coding for a neuron-specific gap junctional protein. J. Membr. Biol. 176, 249–262 (2000).
Srinivas, M. et al. Functional properties of channels formed by the neuronal gap junction protein connexin36. J. Neurosci. 19, 9848–9855 (1999).
Urban, N.N. & Sakmann, B. Reciprocal intraglomerular excitation and intra- and interglomerular lateral inhibition between mouse olfactory bulb mitral cells. J. Physiol. 542, 355–367 (2002).
Didier, A. et al. A dendrodendritic reciprocal synapse provides a recurrent excitatory connection in the olfactory bulb. Proc. Natl. Acad. Sci. USA. 98, 6441–6446 (2001).
Isaacson, J.S. & Strowbridge, B.W. Olfactory reciprocal synapses; dendritic signaling in the CNS. Neuron 20, 749–761 (1998).
Schoppa, N.E., Kinzie, J.M., Sahara, Y., Segerson, T.P. & Westbrook, G.L. Dendrodendritic inhibition in the olfactory bulb is driven by NMDA receptors. J. Neurosci. 18, 6790–6802 (1998).
Schoppa, N.E. & Westbrook, G.L. Regulation of synaptic timing in the olfactory bulb by an A-type potassium current. Nat. Neurosci. 2, 1106–1113 (1999).
Singer, W. Neuronal synchrony: a versatile code for the definition of relations? Neuron 24, 49–65 (1999).
Zou, Z., Horowitz, L.F., Montmayeur, J.P., Snapper, S. & Buck, L.B. Genetic tracing reveals a stereotyped sensory map in the olfactory cortex. Nature 414, 173–179 (2001).
MacLeod, K., Bäcker, A. & Laurent, G. Who reads temporal information contained across synchronized and oscillatory spike trains? Nature 395, 693–698 (1998).
Usrey, W.M., Alonso, J.-M. & Reid, R.C. Synaptic interactions between thalamic inputs to simple cells in cat visual cortex. J. Neurosci. 20, 5461–5467 (2000).
Shadlen, M.N. & Movshon, J.A. Synchrony unbound: a critical evaluation of the temporal binding hypothesis. Neuron 24, 67–77, 111–125 (1999).
Kay, L.M. & Laurent, G. Odor- and context-dependent modulation of mitral cell activity in behaving rats. Nat. Neurosci. 2, 1003–1009 (1999).
Hines, M.L. & Carnevale, N.T. The NEURON simulation environment. Neural Comput. 9, 1179–1209 (1997).
Shen, G.Y., Chen, W.R., Midtgaard, J., Shepherd, G.M. & Hines, M.L. Computational analysis of action potential initiation in mitral cell soma and dendrites based on dual patch recordings. J. Neurophysiol. 82, 3006–3020 (1999).
Acknowledgements
This work was supported by National Institute of Health grant NS26494 to G.L.W. We thank members of the Westbrook lab for helpful discussions.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Rights and permissions
About this article
Cite this article
Schoppa, N., Westbrook, G. AMPA autoreceptors drive correlated spiking in olfactory bulb glomeruli. Nat Neurosci 5, 1194–1202 (2002). https://doi.org/10.1038/nn953
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nn953
This article is cited by
-
Nonlinear dendritic integration of electrical and chemical synaptic inputs drives fine-scale correlations
Nature Neuroscience (2014)
-
Increased Kv1 Channel Expression May Contribute to Decreased sIPSC Frequency Following Chronic Inhibition of NR2B-Containing NMDAR
Neuropsychopharmacology (2012)
-
Patterns of heterogeneous expression of pannexin 1 and pannexin 2 transcripts in the olfactory epithelium and olfactory bulb
Journal of Molecular Histology (2012)
-
Population diversity and function of hyperpolarization-activated current in olfactory bulb mitral cells
Scientific Reports (2011)
-
Gap junctions in olfactory neurons modulate olfactory sensitivity
BMC Neuroscience (2010)