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A large-scale model of the locust antennal lobe

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Abstract

The antennal lobe (AL) is the primary structure within the locust’s brain that receives information from olfactory receptor neurons (ORNs) within the antennae. Different odors activate distinct subsets of ORNs, implying that neuronal signals at the level of the antennae encode odors combinatorially. Within the AL, however, different odors produce signals with long-lasting dynamic transients carried by overlapping neural ensembles, suggesting a more complex coding scheme. In this work we use a large-scale point neuron model of the locust AL to investigate this shift in stimulus encoding and potential consequences for odor discrimination. Consistent with experiment, our model produces stimulus-sensitive, dynamically evolving populations of active AL neurons. Our model relies critically on the persistence time-scale associated with ORN input to the AL, sparse connectivity among projection neurons, and a synaptic slow inhibitory mechanism. Collectively, these architectural features can generate network odor representations of considerably higher dimension than would be generated by a direct feed-forward representation of stimulus space.

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References

  • Ache, B., & Young, J. (2005). Olfaction: diverse species, conserved principles. Neuron, 48, 417–430. doi:10.1016/j.neuron.2005.10.022.

    Article  CAS  PubMed  Google Scholar 

  • Axel, R. (1995). The molecular logic of smell. Scientific American, 273, 154–159.

    Article  CAS  PubMed  Google Scholar 

  • Barbara, G., Zube, C., Rybak, J., Gauthier, M., & Grünewald, B. (2005). Acetylcholine, GABA and glutamate induce ionic currents in cultured antennal lobe neurons of the honeybee, Apis Mellifera. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology, 191, 823–836. doi:10.1007/s00359-005-0007-3.

    Article  Google Scholar 

  • Bazhenov, M., Timofeev, I., Steriade, M., & Sejnowski, T. (1998). Cellular and network models for intrathalamic augmenting responses during 10 Hz Stimulation. Journal of Neurophysiology, 79, 2730–2748.

    CAS  PubMed  Google Scholar 

  • Bazhenov, M., Stopfer, M., Rabinovich, M., Abarbanel, H., Sejnowski, T., & Laurent, G. (2001a). Model of cellular and network mechanisms for odor-evoked temporal patterning in the locust antennal lobe. Neuron, 30, 569–581. doi:10.1016/S0896-6273(01)00286-0.

    Article  CAS  Google Scholar 

  • Bazhenov, M., Stopfer, M., Rabinovich, M., Huerta, R., Abarbanel, H., Sejnowski, T., et al. (2001b). Model of transient oscillatory synchronization in the locust antennal lobe. Neuron, 30, 553–567. doi:10.1016/S0896-6273(01)00284-7.

    Article  CAS  Google Scholar 

  • Bhandawat, V., Olsen, S., Gouwens, N., Schlief, M., & Wilson, R. (2007). Sensory processing in the Drosophila antennal lobe increases reliability and separability of ensemble odor representations. Nature Neuroscience, 10, 1474–1482. doi:10.1038/nn1976.

    Article  CAS  PubMed  Google Scholar 

  • Costanzo, R., & Morrison, E. (1989). Three-dimensional scanning electron microscopic study of the normal hamster olfactory epithelium. Journal of Neurocytology, 18, 381–391. doi:10.1007/BF01190841.

    Article  CAS  PubMed  Google Scholar 

  • de Bruyne, M., Clyne, P., & Carlson, J. (1999). Odor coding in a model olfactory organ: the Drosophila Maxillary Palp. The Journal of Neuroscience, 19, 4520–4532.

    PubMed  Google Scholar 

  • de Bruyne, M., Foster, K., & Carlson, J. (2001). Odor coding in the drosophila antenna. Neuron, 30, 537–552. doi:10.1016/S0896-6273(01)00289-6.

    Article  PubMed  Google Scholar 

  • Destexhe, A., Bal, T., McCormick, D., & Sejnowski, T. (1996). Ionic mechanisms underlying synchronized oscillations and propagating waves in a model of ferret thalamic slices. Journal of Neurophysiology, 76, 2049–2070.

    CAS  PubMed  Google Scholar 

  • Duchamp-Viret, P., Duchamp, A., & Chaput, M. (2000). Peripheral odor coding in the rat and frog: quality and intensity specification. The Journal of Neuroscience, 20, 2383–2390.

    CAS  PubMed  Google Scholar 

  • Dutar, P., & Nicoll, R. (1988). A physiological role for GABAB Receptors in the central nervous system. Nature, 332, 156–158. doi:10.1038/332156a0.

    Article  CAS  PubMed  Google Scholar 

  • Friedrich, R., & Korsching, S. (1997). Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging. Neuron, 18, 737–752. doi:10.1016/S0896-6273(00)80314-1.

    Article  CAS  PubMed  Google Scholar 

  • Friedrich, R., & Laurent, G. (2001). Dynamic optimization of odor representations by slow temporal patterning of mitral cell activity. Science, 291, 889–894. doi:10.1126/science.291.5505.889.

    Article  CAS  PubMed  Google Scholar 

  • Friedrich, R., & Laurent, G. (2004). Dynamics of olfactory bulb input and output activity during odor stimulation in zebrafish. Journal of Neurophysiology, 91, 2658–2669. doi:10.1152/jn.01143.2003.

    Article  PubMed  Google Scholar 

  • Fuss, S., & Korsching, S. (2001). Odorant feature detection: activity mapping of stucture response relationships in the zebrafish olfactory bulb. The Journal of Neuroscience, 21, 8396–8407.

    CAS  PubMed  Google Scholar 

  • Galizia, C., Sachse, S., & Mustaparta, H. (2000). Calcium responses to pheromones and plant odours in the antennal lobe of the male and female moth Heliothis virescens. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology, 186, 1049–1063. doi:10.1007/s003590000156.

    Article  CAS  PubMed  Google Scholar 

  • Gao, Q., Yuan, B., & Chess, A. (2000). Convergent projections of drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nature Neuroscience, 3, 780–785. doi:10.1038/75753.

    Article  CAS  PubMed  Google Scholar 

  • Graziadei, P., & Metcalf, J. (1971). Autoradiographic and ultrastructural observations on the frog’s olfactory mucosa. Z Zellforsch Mikrosk Anat., 116, 305–318. doi:10.1007/BF00330630.

    Article  CAS  PubMed  Google Scholar 

  • Hallem, E., & Carlson, J. (2006). Coding of odors by a receptor repertoire. Cell, 125, 143–160. doi:10.1016/j.cell.2006.01.050.

    Article  CAS  PubMed  Google Scholar 

  • Hansson, B., & Anton, S. (2000). Function and morphology of the antennal lobe: new developments. Annual Review of Entomology, 45, 203–231. doi:10.1146/annurev.ento.45.1.203.

    Article  CAS  PubMed  Google Scholar 

  • Heisenberg, M. (1998). What do the mushroom bodies do for the insect brain? An Introduction. Learning & Memory (Cold Spring Harbor, N.Y.), 5, 1–10.

    CAS  Google Scholar 

  • Hildebrand, J., & Shepherd, G. (1997). Mechanisms of olfactory discrimination : converging evidence for common principles across phyla. Annual Review of Neuroscience, 20, 595–631. doi:10.1146/annurev.neuro.20.1.595.

    Article  CAS  PubMed  Google Scholar 

  • Hildebrand, J., Rossler, W., & Tolbert, L. (1997). Postembryonic development of the olfactory system in the moth manduca sexta: primary-afferent control of glomerular development. Seminars in Cell & Developmental Biology, 8, 163–170. doi:10.1006/scdb.1996.0139.

    Article  CAS  Google Scholar 

  • Hodgkin, A., & Huxley, A. (1952). A quantitative description of membrane current and its application to conduction and excitation in nerve. The Journal of Physiology, 117, 500–544.

    CAS  PubMed  Google Scholar 

  • Homberg, U., Christensen, T., & Hildebrand, J. (1989). Structure and function of the deutocerebrum in insects. Annual Review of Entomology, 34, 477–501. doi:10.1146/annurev.en.34.010189.002401.

    Article  CAS  PubMed  Google Scholar 

  • Huguenard, J., Coulter, D., & McCormick, D. (1991). A fast transient potassium current in thalamic relay neurons. Kinetics of Activation and Inactivation. Journal of Neurophysiology, 66, 1305–1315.

    Google Scholar 

  • Joerges, J., Küttner, A., Galizia, G., & Menzel, R. (1997). Representations of odours and odour mixtures visualized in the honeybee brain. Nature, 387, 285–288. doi:10.1038/387285a0.

    Article  CAS  Google Scholar 

  • Johnson, B., & Leon, M. (2000). Modular representation of odorants in the glomerular layer of the rat olfactory bulb and the effects of stimulus concentration. The Journal of Comparative Neurology, 422, 496–509. doi:10.1002/1096-9861(20000710)422:4<496::AID-CNE2>3.0.CO;2-4.

    Article  CAS  PubMed  Google Scholar 

  • Kenyon, F. (1896). The brain of the bee. A preliminary contribution to the morphology of the nervous system of the arthropoda. The Journal of Comparative Neurology, 6, 133–210. doi:10.1002/cne.910060302.

    Article  Google Scholar 

  • Laurent, G. (1996). Dynamical representation of odors by oscillating and evolving neural assemblies. Trends in Neurosciences, 19, 489–496. doi:10.1016/S0166-2236(96)10054-0.

    Article  CAS  PubMed  Google Scholar 

  • Laurent, G., & Davidowitz, H. (1994). Encoding of olfactory information with oscillating neural assemblies. Science, 265, 1872–1875. doi:10.1126/science.265.5180.1872.

    Article  PubMed  Google Scholar 

  • Laurent, G., & Naraghi, M. (1994). Odorant-induced oscillations in the mushroom bodies of the locust. The Journal of Neuroscience, 14, 2993–3004.

    CAS  PubMed  Google Scholar 

  • Laurent, G., Seymour-Laurent, K., & Johnson, K. (1993). Dendritic excitability and a voltage-gated calcium current in locust nonspiking local interneurons. Journal of Neurophysiology, 69, 1484–1498.

    CAS  PubMed  Google Scholar 

  • Laurent, G., Wehr, M., & Davidowitz, H. (1996). Temporal representations of odors in an olfactory network. The Journal of Neuroscience, 16, 3837–3847.

    CAS  PubMed  Google Scholar 

  • Laurent, G., Stopfer, M., Friedrich, R., Rabinovich, M., Volkovskii, A., & Abarbanel, H. (2001). Odor encoding as an active, dynamical process : experiments, computation, and theory. Annual Review of Neuroscience, 24, 263–297. doi:10.1146/annurev.neuro.24.1.263.

    Article  CAS  PubMed  Google Scholar 

  • Leitch, B., & Laurent, G. (1996). GABAergic synapses in the antennal lobe and mushroom body of the locust olfactory system. The Journal of Comparative Neurology, 372, 487–514. doi:10.1002/(SICI)1096-9861(19960902)372:4<487::AID-CNE1>3.0.CO;2-0.

    Article  CAS  PubMed  Google Scholar 

  • MacLeod, K., & Laurent, G. (1996). Distinct mechanisms for synchronization and temporal patterning of odor-encoding neural assemblies. Science, 274, 976–979. doi:10.1126/science.274.5289.976.

    Article  CAS  PubMed  Google Scholar 

  • MacLeod, K., Bäcker, A., & Laurent, G. (1998). Who reads temporal information contained across synchronized and oscillatory spike trains? Nature, 395, 693–698. doi:10.1038/27201.

    Article  CAS  PubMed  Google Scholar 

  • Malnic, B., Hirono, J., Sato, T., & Buck, L. (1999). Combinatorial receptor codes for odors. Cell, 96, 713–723. doi:10.1016/S0092-8674(00)80581-4.

    Article  CAS  PubMed  Google Scholar 

  • Mazor, O., & Laurent, G. (2005). Transient dynamics versus fixed points in odor representations by locust antennal lobe projection neurons. Neuron, 48, 661–673. doi:10.1016/j.neuron.2005.09.032.

    Article  CAS  PubMed  Google Scholar 

  • Meister, M., & Bonhoeffer, T. (2001). Tuning and topography in an odor map on the rat olfactory bulb. The Journal of Neuroscience, 21, 1351–1360.

    CAS  PubMed  Google Scholar 

  • Mercer, A., & Hildebrand, J. (2002a). Developmental changes in the density of ionic currents in antennal-lobe neurons of the sphinx moth, Manduca Sexta. Journal of Neurophysiology, 87, 2664–2675.

    CAS  Google Scholar 

  • Mercer, A., & Hildebrand, J. (2002b). Developmental changes in the electrophysiological properties and response characteristics of manduca antennal-lobe neurons. Journal of Neurophysiology, 87, 2650–2663.

    Google Scholar 

  • Moulton, D. (1974). Dynamics of cell populations in the olfactory epithelium. Annals of the New York Academy of Sciences, 237, 52–61. doi:10.1111/j.1749-6632.1974.tb49843.x.

    Article  CAS  PubMed  Google Scholar 

  • Ng, M., Roorda, R., Lima, S., Zemelman, B., Morcillo, P., & Miesenbock, G. (2002). Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron, 36, 463–474. doi:10.1016/S0896-6273(02)00975-3.

    Article  CAS  PubMed  Google Scholar 

  • Perez-Orive, J., Mazor, O., Turner, G., Cassenaer, S., Wilson, R., & Laurent, G. (2002). Oscillations and sparsening of odor representations in the mushroom body. Science, 297, 359–365. doi:10.1126/science.1070502.

    Article  CAS  PubMed  Google Scholar 

  • Perez-Orive, J., Bazhenov, M., & Laurent, G. (2004). Intrinsic and circuit properties favor coincidence detection for decoding oscillatory input. The Journal of Neuroscience, 24, 6037–6047. doi:10.1523/JNEUROSCI.1084-04.2004.

    Article  CAS  PubMed  Google Scholar 

  • Reisenman, C., Christensen, T., Francke, W., & Hildebrand, J. (2004). Enantioselectivity of projection neurons innervating identified olfactory glomeruli. The Journal of Neuroscience, 24, 2602–2611. doi:10.1523/JNEUROSCI.5192-03.2004.

    Article  CAS  PubMed  Google Scholar 

  • Rubin, B., & Katz, L. (1999). Optical imaging of odorant representations in the mammalian olfactory bulb. Neuron, 23, 499–511. doi:10.1016/S0896-6273(00)80803-X.

    Article  CAS  PubMed  Google Scholar 

  • Sachse, S., & Galizia, C. (2002). Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. Journal of Neurophysiology, 87, 1106–1117.

    PubMed  Google Scholar 

  • Sachse, S., Rappert, A., & Galizia, C. (1999). The spatial representation of chemical structures in the antennal lobes of honeybees: steps towards the olfactory code. The European Journal of Neuroscience, 11, 3970–3982. doi:10.1046/j.1460-9568.1999.00826.x.

    Article  CAS  PubMed  Google Scholar 

  • Sivan, E., & Kopell, N. (2004). Mechanism and circuitry for clustering and fine discrimination of odors in insects. Proceedings of the National Academy of Sciences of the United States of America, 101, 17861–17866. doi:10.1073/pnas.0407858101.

    Article  CAS  PubMed  Google Scholar 

  • Sivan, E., & Kopell, N. (2006). Oscillations and Slow Patterning in the Antennal Lobe. Journal of Computational Neuroscience, 20, 85–96. doi:10.1007/s10827-006-4087-z.

    Article  PubMed  Google Scholar 

  • Sloper, J., & Powell, T. (1978). Ultrastructural features of the sensori-motor cortex of the primate. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 285, 124–139.

    Google Scholar 

  • Stopfer, M., Bhagavan, S., Smith, B., & Laurent, G. (1997). Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature, 390, 70–74. doi:10.1038/36335.

    Article  CAS  PubMed  Google Scholar 

  • Strausfeld, N., Hansen, L., Li, Y., Gomez, R., & Ito, K. (1998). Evolution, discovery, and interpretations of arthropod mushroom bodies. Learning & Memory (Cold Spring Harbor, N.Y.), 5, 11–37.

    CAS  Google Scholar 

  • Treloar, H., Feinstein, P., Mombaerts, P., & Greer, C. (2002). Specificity of glomerular targeting by olfactory sensory axons. The Journal of Neuroscience, 22, 2469–2477.

    CAS  PubMed  Google Scholar 

  • Vickers, N., & Christensen, T. (1998). A combinatorial model of odor discrimination using a small array of contiguous, chemically defined glomeruli. Annals of the New York Academy of Sciences, 855, 514–516. doi:10.1111/j.1749-6632.1998.tb10617.x.

    Article  CAS  PubMed  Google Scholar 

  • Vickers, N., Christensen, T., & Hildebrand, J. (1998). Combinatorial odor discrimination in the brain: attractive and antagonistic odor blends are represented in distinct combinations of uniquely identifiable glomeruli. The Journal of Comparative Neurology, 400, 35–36. doi:10.1002/(SICI)1096-9861(19981012) 400:1<35::AID-CNE3>3.0.CO;2-U.

    Article  CAS  PubMed  Google Scholar 

  • Vosshall, L., Wong, A., & Axel, R. (2000). An olfactory sensory map in the fly brain. Cell, 102, 147–159. doi:10.1016/S0092-8674(00)00021-0.

    Article  CAS  PubMed  Google Scholar 

  • Wachowiak, M., & Cohen, L. (2001). Representation of odorants by receptor neuron input to the mouse olfactory bulb. Neuron, 32, 723–735. doi:10.1016/S0896-6273(01)00506-2.

    Article  CAS  PubMed  Google Scholar 

  • Wang, J., Wong, A., Flores, J., Vosshall, L., & Axel, R. (2003). Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell, 112, 271–282. doi:10.1016/S0092-8674(03)00004-7.

    Article  CAS  PubMed  Google Scholar 

  • Wehr, M., & Laurent, G. (1999). Relationship between afferent and central temporal patterns in the locust olfactory system. The Journal of Neuroscience, 19, 381–390.

    CAS  PubMed  Google Scholar 

  • Wilson, R., & Mainen, Z. (2006). Early events in olfactory processing. Annual Review of Neuroscience, 29, 163–201. doi:10.1146/annurev.neuro.29.051605.112950.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. The Sackler Institute of Graduate Biomedical Sciences, NYU School of Medicine, 550 First Avenue, New York, NY, 10016, USA

    Mainak Patel

  2. Courant Institute of Mathematical Sciences, New York University, 251 Mercer Street, New York, NY, 10012-1185, USA

    Aaditya V. Rangan & David Cai

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  1. Mainak Patel
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  2. Aaditya V. Rangan
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Correspondence to Aaditya V. Rangan.

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Patel, M., Rangan, A.V. & Cai, D. A large-scale model of the locust antennal lobe. J Comput Neurosci 27, 553–567 (2009). https://doi.org/10.1007/s10827-009-0169-z

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