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Adaptive regulation of sparseness by feedforward inhibition

Abstract

In the mushroom body of insects, odors are represented by very few spikes in a small number of neurons, a highly efficient strategy known as sparse coding. Physiological studies of these neurons have shown that sparseness is maintained across thousand-fold changes in odor concentration. Using a realistic computational model, we propose that sparseness in the olfactory system is regulated by adaptive feedforward inhibition. When odor concentration changes, feedforward inhibition modulates the duration of the temporal window over which the mushroom body neurons may integrate excitatory presynaptic input. This simple adaptive mechanism could maintain the sparseness of sensory representations across wide ranges of stimulus conditions.

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Figure 1: Network structure.
Figure 2: Oscillatory dynamics of antennal lobe neurons for different odor concentrations.
Figure 3: Collective dynamics of neurons in the modeled antennal lobe.
Figure 4: Collective dynamics of neurons in the modeled mushroom body.
Figure 5: PN and LHI responses for different odor concentrations.
Figure 6: Effect of adaptive feedforward inhibition of KC activity.
Figure 7: Phase advance of LHIs maintains the sparseness of KC activity.
Figure 8: Role of feedforward inhibition in a minimal neural circuit.

References

  1. Gross-Isseroff, R. & Lancet, D. Concentration-dependent changes of perceived odor quality. Chem. Senses 13, 191–204 (1988).

    Article  Google Scholar 

  2. Bhagavan, S. & Smith, B.H. Olfactory conditioning in the honey bee, Apis mellifera: effects of odor intensity. Physiol. Behav. 61, 107–117 (1997).

    CAS  PubMed  Article  Google Scholar 

  3. Stopfer, M., Jayaraman, V. & Laurent, G. Intensity versus identity coding in an olfactory system. Neuron 39, 991–1004 (2003).

    CAS  PubMed  Article  Google Scholar 

  4. Laurent, G. Olfactory network dynamics and the coding of multidimensional signals. Nat. Rev. Neurosci. 3, 884–895 (2002).

    CAS  PubMed  Article  Google Scholar 

  5. Kanerva, P. Sparse Distributed Memory, (Bradford Books, Boston, 1988).

    Google Scholar 

  6. Olshausen, B.A. & Field, D.J. Sparse coding of sensory inputs. Curr. Opin. Neurobiol. 14, 481–487 (2004).

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  8. Laurent, G., Wehr, M. & Davidowitz, H. Temporal representations of odors in an olfactory network. J. Neurosci. 16, 3837–3847 (1996).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  9. Perez-Orive, J. et al. Oscillations and sparsening of odor representations in the mushroom body. Science 297, 359–365 (2002).

    CAS  PubMed  Article  Google Scholar 

  10. Perez-Orive, J., Bazhenov, M. & Laurent, G. Intrinsic and circuit properties favor coincidence detection for decoding oscillatory input. J. Neurosci. 24, 6037–6047 (2004).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  11. Pouille, F. & Scanziani, M. Enforcement of temporal fidelity in pyramidal cells by somatic feedforward inhibition. Science 293, 1159–1163 (2001).

    CAS  PubMed  Article  Google Scholar 

  12. Mittmann, W., Koch, U. & Hausser, M. Feedforward inhibition shapes the spike output of cerebellar Purkinje cells. J. Physiol. (Lond.) 563, 369–378 (2005).

    CAS  Article  Google Scholar 

  13. Anton, S. & Homberg, U. Antennal lobe structure. in Insect Olfaction (ed. Hansson, B.S.) (Springer, Berlin, 1999).

    Google Scholar 

  14. Matthews, H.R. & Reisert, J. Calcium, the two-faced messenger of olfactory transduction and adaptation. Curr. Opin. Neurobiol. 13, 469–475 (2003).

    CAS  PubMed  Article  Google Scholar 

  15. Anderson, P., Hansson, B.S. & Löfqvist, J. Plant-odour–specific receptor neurones on the antennae of female and male Spodoptera littoralis. Physiol. Entomol. 20, 189–198 (1995).

    CAS  Article  Google Scholar 

  16. Hallem, E.A. & Carlson, J.R. Coding of odors by a receptor repertoire. Cell 125, 143–160 (2006).

    CAS  PubMed  Article  Google Scholar 

  17. Hallem, E.A., Ho, M.G. & Carlson, J.R. The molecular basis of odor coding in the Drosophila antenna. Cell 117, 965–979 (2004).

    CAS  PubMed  Article  Google Scholar 

  18. Ernst, K.D., Boeckh, J. & Boeckh, V. A neuroanatomical study on the organization of the central antennal pathways in insects. Cell Tissue Res. 176, 285–306 (1977).

    CAS  PubMed  Article  Google Scholar 

  19. MacLeod, K., Backer, A. & Laurent, G. Who reads temporal information contained across synchronized and oscillatory spike trains? Nature 395, 693–698 (1998).

    CAS  PubMed  Article  Google Scholar 

  20. MacLeod, K. & Laurent, G. Distinct mechanisms for synchronization and temporal patterning of odor-encoding neural assemblies. Science 274, 976–979 (1996).

    CAS  PubMed  Article  Google Scholar 

  21. Laurent, G. & Davidowitz, H. Encoding of olfactory information with oscillating neural assemblies. Science 265, 1872–1875 (1994).

    CAS  PubMed  Article  Google Scholar 

  22. Bazhenov, M. et al. Model of cellular and network mechanisms for odor-evoked temporal patterning in the locust antennal lobe. Neuron 30, 569–581 (2001).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  23. Bazhenov, M. et al. Model of transient oscillatory synchronization in the locust antennal lobe. Neuron 30, 553–567 (2001).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  24. Margrie, T.W., Sakmann, B. & Urban, N.N. Action potential propagation in mitral cell lateral dendrites is decremental and controls recurrent and lateral inhibition in the mammalian olfactory bulb. Proc. Natl. Acad. Sci. USA 98, 319–324 (2001).

    CAS  PubMed  Article  Google Scholar 

  25. Jortner, R.A., Farivar, S.S. & Laurent, G. A simple connectivity scheme for sparse coding in an olfactory system. J. Neurosci. 27, 1659–1669 (2007).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  26. Mazor, O. & Laurent, G. Transient dynamics versus fixed points in odor representations by locust antennal lobe projection neurons. Neuron 48, 661–673 (2005).

    CAS  PubMed  Article  Google Scholar 

  27. Marr, D. A theory of cerebellar cortex. J. Physiol. (Lond.) 202, 437–470 (1969).

    CAS  Article  Google Scholar 

  28. Salinas, E. & Sejnowski, T.J. Impact of correlated synaptic input on output firing rate and variability in simple neuronal models. J. Neurosci. 20, 6193–6209 (2000).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  29. Stopfer, M., Bhagavan, S., Smith, B.H. & Laurent, G. Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390, 70–74 (1997).

    CAS  PubMed  Article  Google Scholar 

  30. Konig, P., Engel, A.K. & Singer, W. Integrator or coincidence detector? The role of the cortical neuron revisited. Trends Neurosci. 19, 130–137 (1996).

    CAS  PubMed  Article  Google Scholar 

  31. Hopfield, J.J. Pattern recognition computation using action potential timing for stimulus representation. Nature 376, 33–36 (1995).

    CAS  PubMed  Article  Google Scholar 

  32. Buzsaki, G. Feedforward inhibition in the hippocampal formation. Prog. Neurobiol. 22, 131–153 (1984).

    CAS  PubMed  Article  Google Scholar 

  33. Blitz, D.M. & Regehr, W.G. Timing and specificity of feed-forward inhibition within the LGN. Neuron 45, 917–928 (2005).

    CAS  PubMed  Article  Google Scholar 

  34. Sun, Q.Q., Huguenard, J.R. & Prince, D.A. Barrel cortex microcircuits: thalamocortical feedforward inhibition in spiny stellate cells is mediated by a small number of fast-spiking interneurons. J. Neurosci. 26, 1219–1230 (2006).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. Destexhe, A., Mainen, Z.F. & Sejnowski, T.J. Synthesis of models for excitable membranes, synaptic transmission and neuromodulation using a common kinetic formalism. J. Comput. Neurosci. 1, 195–230 (1994).

    CAS  PubMed  Article  Google Scholar 

  36. Wilson, R.I. & Laurent, G. Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J. Neurosci. 25, 9069–9079 (2005).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  37. Rulkov, N.F., Timofeev, I. & Bazhenov, M. Oscillations in large-scale cortical networks: map-based model. J. Comput. Neurosci. 17, 203–223 (2004).

    CAS  PubMed  Article  Google Scholar 

  38. Bazhenov, M., Rulkov, N.F., Fellous, J.M. & Timofeev, I. Role of network dynamics in shaping spike-timing reliability. Phys. Rev. E 72, 041903 (2005).

    Article  Google Scholar 

  39. Bazhenov, M., Stopfer, M., Sejnowski, T.J. & Laurent, G. Fast odor learning improves reliability of odor responses in the locust antennal lobe. Neuron 46, 483–492 (2005).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  40. Laurent, G. Dynamical representation of odors by oscillating and evolving neural assemblies. Trends Neurosci. 19, 489–496 (1996).

    CAS  PubMed  Article  Google Scholar 

  41. Wehr, M. & Laurent, G. Relationship between afferent and central temporal patterns in the locust olfactory system. J. Neurosci. 19, 381–390 (1999).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  42. Laurent, G. & Naraghi, M. Odorant-induced oscillations in the mushroom bodies of the locust. J. Neurosci. 14, 2993–3004 (1994).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  43. Stopfer, M. & Laurent, G. Short-term memory in olfactory network dynamics. Nature 402, 664–668 (1999).

    CAS  PubMed  Article  Google Scholar 

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Acknowledgements

This work was supported by grants from the US National Institute of Deafness and other Communication Disorders (C.A., G.L. and M.B.), the National Science Foundation (G.L.) and a US National Institute of Child Health and Human Development intramural award (M.S.).

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Correspondence to Maxim Bazhenov.

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Assisi, C., Stopfer, M., Laurent, G. et al. Adaptive regulation of sparseness by feedforward inhibition. Nat Neurosci 10, 1176–1184 (2007). https://doi.org/10.1038/nn1947

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