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Non-classical receptive field mediates switch in a sensory neuron's frequency tuning

A Corrigendum to this article was published on 26 June 2003


Animals have developed stereotyped communication calls to which specific sensory neurons are well tuned1,2. These communication calls must be discriminated from environmental signals such as those produced by prey. Sensory systems might have evolved neural circuitry to encode both categories. In weakly electric fish, prey and communication signals differ in their spatial extent and frequency content3,4. Here we show that stimuli of different spatial extents mimicking prey and communication signals cause a switch in the frequency tuning and spike-timing precision of electrosensory pyramidal neurons, resulting in the selective and optimal encoding of both stimulus categories. As in other sensory systems5, pyramidal neurons respond only to stimuli located within a restricted region of space known as the classical receptive field (CRF)6. In some systems, stimulation outside the CRF but within a non-classical receptive field (nCRF) can modulate the neural response to CRF stimulation even though nCRF stimulation alone fails to elicit responses7,8. We show that pyramidal neurons possess a nCRF and that it can modulate the response to CRF stimuli to induce this neurobiological switch in frequency tuning.

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Figure 1: ELL pyramidal neurons display differential frequency tuning to local and global stimulation geometries.
Figure 2: Spike timing reliability and precision under local and global stimulation geometries.
Figure 3: The nCRF mediates pyramidal neuron frequency tuning.

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  1. Rieke, F., Bodnar, D. A. & Bialek, W. Naturalistic stimuli increase the rate and efficiency of information transmission by primary auditory afferents. Proc. R. Soc. Lond. B 262, 259–265 (1995)

    Article  ADS  CAS  Google Scholar 

  2. Machens, C. K. et al. Representation of acoustic communication signals by insect auditory neurons. J. Neurosci. 21, 3215–3227 (2001)

    Article  CAS  Google Scholar 

  3. Nelson, M. E. & MacIver, M. A. Prey capture in the weakly electric fish Apteronotus leptorhynchus: sensory acquisition strategies and electrosensory consequences. J. Exp. Biol. 202, 1195–1203 (1999)

    CAS  PubMed  Google Scholar 

  4. Zupanc, G. K. H. & Maler, L. Evoked chirping in the weakly electric fish Apteronotus leptorhynchus: a quantitative biophysical analysis. Can. J. Zool. 71, 2301–2310 (1993)

    Article  Google Scholar 

  5. Hubel, D. H. & Wiesel, T. N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. (Lond.) 160, 106–154 (1962)

    Article  CAS  Google Scholar 

  6. Bastian, J., Chacron, M. J. & Maler, L. Receptive field organization determines pyramidal cell stimulus-encoding capability and spatial stimulus selectivity. J. Neurosci. 22, 4577–4590 (2002)

    Article  CAS  Google Scholar 

  7. Sillito, A. M., Grieve, K. L., Jones, H. E., Cudeiro, J. & Davis, J. Visual cortical mechanisms detecting focal orientation discontinuities. Nature 378, 492–496 (1995)

    Article  ADS  CAS  Google Scholar 

  8. Vinje, W. & Gallant, J. L. Sparse Coding and decorrelation in primary visual cortex during natural vision. Science 287, 1273–1276 (2000)

    Article  ADS  CAS  Google Scholar 

  9. Simoncelli, E. P. & Olshausen, B. A. Natural image statistics and neural representation. Annu. Rev. Neurosci. 24, 1193–1216 (2001)

    Article  CAS  Google Scholar 

  10. Voss, R. F. & Clarke, J. ‘1/f noise’ in music: music from 1/f noise. J. Acoust. Soc. Am. 63, 258–263 (1978)

    Article  ADS  Google Scholar 

  11. Bastian, J. Electrolocation. I. How the electroreceptors of Apteronotus albifrons code for moving objects and other electrical stimuli. J. Comp. Physiol. A 144, 465–479 (1981)

    Article  Google Scholar 

  12. Gabbiani, F., Metzner, W., Wessel, R. & Koch, C. From stimulus encoding to feature extraction in weakly electric fish. Nature 384, 564–567 (1996)

    Article  ADS  CAS  Google Scholar 

  13. Maler, L., Sas, E. K. & Rogers, J. The cytology of the posterior lateral line lobe of high frequency weakly electric fish (Gymnotoidei): Dendritic differentiation and synaptic specificity in a simple cortex. J. Comp. Neurol. 195, 87–139 (1981)

    Article  CAS  Google Scholar 

  14. Rieke, F., Warland, D., de Ruyter van Steveninck, R. R. & Bialek, W. Spikes: Exploring the Neural Code (MIT, Cambridge, Massachusetts, 1996)

    MATH  Google Scholar 

  15. Borst, A. & Theunissen, F. Information theory and neural coding. Nature Neurosci. 2, 947–957 (1999)

    Article  CAS  Google Scholar 

  16. Mainen, Z. F. & Sejnowski, T. J. Reliability of spike timing in neocortical neurons. Science 268, 1503–1506 (1995)

    Article  ADS  CAS  Google Scholar 

  17. de Ruyter van Steveninck, R. R., Lewen, G. D., Strong, S. P., Koberle, R. & Bialek, W. Reproducibility and variability in neural spike trains. Science 275, 1805–1808 (1997)

    Article  CAS  Google Scholar 

  18. Maler, L. & Mugnaini, E. Correlating gamma-aminobutyric acidergic circuits and sensory function in the electrosensory lateral line lobe of a gymnotiform fish. J. Comp. Neurol. 345, 224–252 (1994)

    Article  CAS  Google Scholar 

  19. Berman, N. J. & Maler, L. Neural architecture of the electrosensory lateral line lobe: Adaptations for coincidence detection, a sensory searchlight and frequency-dependent adaptive filtering. J. Exp. Biol. 202, 1243–1253 (1999)

    CAS  PubMed  Google Scholar 

  20. Crampton, W. G. R. Electric signal design and habitat preferences in a species rich assembly of gymnotiform fishes from the upper Amazon basin. Anais Acad. Bras. Cienc. 70, 805–847 (1998)

    Google Scholar 

  21. Zhang, H., Xu, J. & Feng, A. S. Effects of GABA-mediated inhibition on direction-dependent frequency tuning in the frog inferior colliculus. J. Comp. Physiol. 184, 85–98 (1999)

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  23. Doiron, B., Chacron, M. J., Maler, L., Longtin, A. & Bastian, J. Inhibitory feedback required for network burst responses to communication but not prey stimuli. Nature 421, 539–543 (2003)

    Article  ADS  CAS  Google Scholar 

  24. Carr, C. E., Maler, L. & Sas, E. Peripheral organization and central projections of the electrosensory organs in gymnotiform fish. J. Comp. Neurol. 211, 139–153 (1982)

    Article  CAS  Google Scholar 

  25. Heiligenberg, W. & Dye, J. Labelling of electrosensory afferents in a gymnotid fish by intracellular injection of HRP: The mystery of multiple maps. J. Comp. Physiol. A 148, 287–296 (1982)

    Article  Google Scholar 

  26. Metzner, W. & Heiligenberg, W. The coding of signals in the electric communication of the gymnotiform fish Eigenmannia: From electroreceptors to neurons in the torus semicircularis of the midbrain. J. Comp. Physiol. A 169, 135–150 (1991)

    Article  CAS  Google Scholar 

  27. Metzner, W. & Juranek, J. A sensory brain map for each behavior? Proc. Natl Acad. Sci. USA 26, 14798–14803 (1997)

    Article  ADS  Google Scholar 

  28. Heiligenberg, W. Neural Nets in Electric Fish (MIT, Cambridge, Massachusetts, 1991)

    Google Scholar 

  29. Bastchelet, E. Circular Statistics in Biology (Academic, New York, 1981)

    Google Scholar 

  30. Gabbiani, F. Coding of time varying signals in spike trains of linear and half-wave rectifying neurons. Network Comput. Neural Sys. 7, 61–85 (1996)

    MATH  Google Scholar 

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We thank A.-M. Oswald, J. Lewis and B. Lindner for their reading the manuscript. This research was supported by NSERC (M.J.C., B.D., A.L.), CIHR (L.M., A.L.) and NIH (J.B.).

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Correspondence to Maurice J. Chacron.

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Chacron, M., Doiron, B., Maler, L. et al. Non-classical receptive field mediates switch in a sensory neuron's frequency tuning. Nature 423, 77–81 (2003).

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