Skip to main content

Advertisement

SpringerLink
Log in

From stimulus estimation to combination sensitivity: encoding and processing of amplitude and timing information in parallel, convergent sensory pathways

  • Published:
Journal of Computational Neuroscience Aims and scope Submit manuscript

Abstract

Information theoretical approaches to sensory processing in electric fish have focused on the encoding of amplitude modulations in a single sensory pathway in the South American gymnotiforms. To assess the generality of these studies, we investigated the encoding of amplitude and phase modulations in the distantly related African fish Gymnarchus. In both the amplitude- and time-coding pathways, primary afferents accurately estimated the time course of random modulations whereas hindbrain neurons extracted information about specific stimulus features. Despite exhibiting a clear preference for encoding amplitude or phase, afferents and hindbrain neurons could encode significant amounts of modulation of their nonpreferred attribute. Although no increase in feature extraction performance occurred where the two pathways converge in the midbrain, neurons there were increasingly sensitive to simultaneous modulation of both attributes. A shift from accurate stimulus estimation in the periphery to increasingly sparse representations of specific features appears to be a general strategy in electrosensory processing.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

References

  • Bastian, J. (1986a). Gain control in the electrosensory system mediated by descending inputs to the electrosensory lateral line lobe. Journal of Neuroscience, 6, 553–562.

    PubMed  CAS  Google Scholar 

  • Bastian, J. (1986b). Gain control in the electrosensory system: A role for the descending projections to the electrosensory lateral line lobe. Journal of Comparative Physiology A, 158, 505–515.

    Article  CAS  Google Scholar 

  • Bastian, J. (1999). Plasticity of feedback inputs in the apteronotid electrosensory system. Journal of Experimental Biology, 202, 1327–1337.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Batschelet, E. (1981). Circular statistics in biology. New York: Academic Press.

    Google Scholar 

  • Bell, C., & Maler, L. (2005). Central neuroanatomy of electrosensory systems in fish. In T. H. Bullock, C. D. Hopkins, A. N. Popper, & R. R. Fay (Eds.), Electroreception (pp. 68–111). New York: Springer.

    Chapter  Google Scholar 

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

    PubMed  Google Scholar 

  • Bialek, W., Rieke, F., de Ruyter van Steveninck, R. R., & Warland, D. (1991). Reading a neural code. Science, 252, 1854–1857.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bullock, T. H., Behrend, K., & Heiligenberg, W. (1975). Comparison of the jamming avoidance responses in gymnotoid and gymnarchid electric fish: A case of convergent evolution of behavior and its sensory basis. Journal of Comparative Physiology, 103, 97–121.

    Article  Google Scholar 

  • Bullock, T. H., Bodznick, D. A., & Northcutt, R. G. (1983). The phylogenetic distribution of electroreception: Evidence for convergent evolution of a primitive vertebrate sense modality. Brain Research Reviews, 6, 25–46.

    Article  Google Scholar 

  • Carlson, B. A., & Kawasaki, M. (2004). Nonlinear response properties of combination-sensitive electrosensory neurons in the midbrain of Gymnarchus niloticus. Journal of Neuroscience, 24, 8039–8048.

    Article  PubMed  CAS  Google Scholar 

  • Carlson, B. A., & Kawasaki, M. (2006a). Ambiguous encoding of stimuli by primary sensory afferents causes a lack of independence in the perception of multiple stimulus attributes. Journal of Neuroscience, 26, 9173–9183.

    Article  PubMed  CAS  Google Scholar 

  • Carlson, B. A., & Kawasaki, M. (2006b). Stimulus selectivity is enhanced by voltage-dependent conductances in combination-sensitive neurons. Journal of Neurophysiology, 96, 3362–3377.

    Article  PubMed  Google Scholar 

  • Carlson, B. A., & Kawasaki, M. (2007). Behavioral responses to jamming and ‘phantom’ jamming stimuli in the weakly electric fish Eigenmannia. Journal of Comparative Physiology A, 193, 927–941.

    Article  Google Scholar 

  • Carr, C. E., Heiligenberg, W., & Rose, G. J. (1986a). A time-comparison circuit in the electric fish Eigenmannia midbrain I. Behavior and physiology. Journal of Neuroscience, 6, 107–119.

    PubMed  CAS  Google Scholar 

  • Carr, C. E., & Maler, L. (1986). Electroreception in gymnotiform fish: Central anatomy and physiology. In T. H. Bullock & W. Heiligenberg (Eds.), Electroreception (pp. 319–373). New York: John Wiley & Sons.

    Google Scholar 

  • Carr, C. E., Maler, L., & Taylor, B. (1986b). A time-comparison circuit in the electric fish Eigenmannia midbrain II. Functional morphology. Journal of Neuroscience, 6, 1372–1383.

    PubMed  CAS  Google Scholar 

  • Chacron, M. (2006). Nonlinear information processing in a model sensory system. Journal of Neurophysiology, 95, 2933–2946.

    Article  PubMed  Google Scholar 

  • Chacron, M., Doiron, B., Maler, L., Longtin, A., & Bastian, J. (2003). Non-classical receptive field mediates switch in a sensory neuron’s frequency tuning. Nature, 423, 77–81.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Fortune, E. (2006). The decoding of electrosensory systems. Current Opinion in Neurobiology, 16, 474–480.

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Gabbiani, F., & Koch, C. (1998). Principles of spike train analysis. In C. Koch & I. Segev (Eds.), Methods in neuronal modeling: From ions to networks (pp. 313–360). Cambridge, MA: The MIT Press.

    Google Scholar 

  • Gabbiani, F., & Metzner, W. (1999). Encoding and processing of sensory information in neuronal spike trains. Journal of Experimental Biology, 202, 1267–1279.

    PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Green, D., & Swets, J. (1966). Signal detection theory and psychophysics. Huntington, NY: Robert E. Krieger Publishing Company.

    Google Scholar 

  • Heiligenberg, W. (1991). Neural nets in electric fish. Cambridge: MIT Press.

    Google Scholar 

  • Heiligenberg, W., & Partridge, B. L. (1981). How electroreceptors encode JAR-eliciting stimulus regimes: Reading trajectories in a phase-amplitude plane. Journal of Comparative Physiology, 142, 295–308.

    Article  Google Scholar 

  • Hopkins, C. D. (1995). Convergent designs for electrogenesis and electroreception. Current Opinion in Neurobiology, 5, 769–777.

    Article  PubMed  CAS  Google Scholar 

  • Kawasaki, M. (1993). Independently evolved jamming avoidance responses employ identical computational algorithms: A behavioral study of the African electric fish, Gymnarchus niloticus. Journal of Comparative Physiology A, 173, 9–22.

    Article  CAS  Google Scholar 

  • Kawasaki, M. (2005). Physiology of tuberous electrosensory systems. In T. H. Bullock, C. D. Hopkins, A. N. Popper, & R. R. Fay (Eds.), Electroreception (pp. 154–194). New York: Springer.

    Chapter  Google Scholar 

  • Kawasaki, M., & Guo, Y. X. (1996). Neuronal circuitry for comparison of timing in the electrosensory lateral line lobe of the African wave-type electric fish Gymnarchus niloticus. Journal of Neuroscience, 16, 380–391.

    PubMed  CAS  Google Scholar 

  • Kawasaki, M., & Guo, Y. X. (1998). Parallel projection of amplitude and phase information from the hindbrain to the midbrain of the African electric fish Gymnarchus niloticus. Journal of Neuroscience, 18, 7599–7611.

    PubMed  CAS  Google Scholar 

  • Kawasaki, M., & Guo, Y. X. (2002). Emergence of temporal-pattern sensitive neurons in the midbrain of weakly electric fish Gymnarchus niloticus. Journal of Physiology—Paris, 96, 531–537.

    Google Scholar 

  • Knudsen, E. I., & Konishi, M. (1978). A neural map of auditory space in the owl. Science, 200, 795–797.

    Article  PubMed  CAS  Google Scholar 

  • Krahe, R., & Gabbiani, F. (2004). Burst firing in sensory systems. Nature Reviews Neuroscience, 5, 13–23.

    Article  PubMed  CAS  Google Scholar 

  • Krahe, R., Kreiman, G., Gabbiani, F., Koch, C., & Metzner, W. (2002). Stimulus encoding and feature extraction by multiple sensory neurons. Journal of Neuroscience, 22, 2374–2382.

    PubMed  CAS  Google Scholar 

  • Kreiman, G., Krahe, R., Metzner, W., Koch, C., & Gabbiani, F. (2000). Robustness and variability of neuronal coding by amplitude-sensitive afferents in the weakly electric fish Eigenmannia. Journal of Neurophysiology, 84, 189–204.

    PubMed  CAS  Google Scholar 

  • Lauder, G., & Liem, K. (1983). Patterns of diversity and evolution in ray-finned fishes. In R. Northcutt & R. Davis (Eds.), Fish neurobiology (pp. 1–24). Ann Arbor: University of Michigan Press.

    Google Scholar 

  • Macmillan, N., & Creelman, C. (2004). Detection theory: A user’s guide. Mahwah, NJ: Lawrence Erlbaum Associates.

    Google Scholar 

  • Maler, L., Sas, E. K. B., & Rogers, J. (1981). The cytology of the posterior lateral line lobe of high frequency weakly electric fish (Gymnotidae). Dendritic differentiation and synaptic specificity in a simple cortex. Journal of Comparative Neurology, 195, 87–140.

    Article  PubMed  CAS  Google Scholar 

  • Mathieson, W. B., Heiligenberg, W., & Maler, L. (1987). Ultrastructural studies of physiologically identified electrosensory afferent synapses in the gymnotiform fish, Eigenmannia. Journal of Comparative Neurology, 255, 526–537.

    Article  PubMed  CAS  Google Scholar 

  • Matsushita, A., & Kawasaki, M. (2004). Unitary giant synapses embracing a single neuron at the convergent site of time-coding pathways of an electric fish, Gymnarchus niloticus. Journal of Comparative Neurology, 472, 140–155.

    Article  PubMed  Google Scholar 

  • Matsushita, M., & Kawasaki, M. (2005). Neuronal sensitivity to microsecond time disparities in the electrosensory system of Gymnarchus niloticus. Journal of Neuroscience, 25, 11424–11432.

    Article  PubMed  CAS  Google Scholar 

  • McLachlan, G. (2004). Discriminant analysis and statistical pattern recognition. New York: Wiley.

    Google Scholar 

  • Mehaffey, W., Doiron, B., Maler, L., & Turner, R. (2005). Deterministic multiplicative gain control with active dendrites. Journal of Neuroscience, 25, 9968–9977.

    Article  PubMed  CAS  Google Scholar 

  • Merigan, W., & Maunsell, J. (1993). How parallel are the primate visual pathways? Annual Review of Neuroscience, 16, 369–402.

    Article  PubMed  CAS  Google Scholar 

  • Metzner, W., Koch, C., Wessel, R., & Gabbiani, F. (1998). Feature extraction by burst-like spike patterns in multiple sensory maps. Journal of Neuroscience, 18, 2283–2300.

    PubMed  CAS  Google Scholar 

  • Middleton, J., Longtin, A., Benda, J., & Maler, L. (2006). The cellular basis for parallel neural transmission of a high-frequency stimulus and its low-frequency envelope. Proceedings of the National Academy of Sciences of the United States of America, 103, 14596–14601.

    Article  PubMed  CAS  Google Scholar 

  • Nelson, M. E., & MacIver, M. A. (1999). Prey capture in the weakly electric fish Apteronotus albifrons: Sensory acquisition strategies and electrosensory consequences. Journal of Experimental Biology, 202, 1195–1203.

    PubMed  CAS  Google Scholar 

  • Nelson, M. E., MacIver, M. A., & Coombs, S. (2002). Modeling electrosensory and mechanosensory images during the predatory behavior of weakly electric fish. Brain Behavior and Evolution, 59, 199–210.

    Article  Google Scholar 

  • Oswald, A., Chacron, M., Doiron, B., Bastian, J., & Maler, L. (2004). Parallel processing of sensory input by bursts and isolated spikes. Journal of Neuroscience, 24, 4351–4362.

    Article  PubMed  CAS  Google Scholar 

  • Oswald, A., Doiron, B., & Maler, L. (2007). Interval coding. I. Burst interspike intervals as indicators of stimulus intensity. Journal of Neurophysiology, 97, 2731–2743.

    Article  PubMed  Google Scholar 

  • Peña, J. L., & Konishi, M. (2001). Auditory spatial receptive fields created by multiplication. Science, 292, 249–252.

    Article  PubMed  Google Scholar 

  • Rees, A., & Palmer, A. R. (1989). Neuronal responses to amplitude-modulated and pure tone stimuli in the guinea pig inferior colliculus, and their modification by broadband noise. Journal of the Acoustical Society of America, 85, 1978–1994.

    Article  PubMed  CAS  Google Scholar 

  • Roddey, J. C., Girish, B., & Miller, J. P. (2000). Assessing the performance of neural encoding models in the presence of noise. Journal of Computational Neuroscience, 8, 95–112.

    Article  PubMed  CAS  Google Scholar 

  • Rose, G. J., & Fortune, E. S. (1996). New techniques for making whole-cell recordings from CNS neurons in vivo. Neuroscience Research, 26, 89–94.

    PubMed  CAS  Google Scholar 

  • Sawtell, N., Williams, A., & Bell, C. (2005). From sparks to spikes: Information processing in the electrosensory systems of fish. Current Opinion in Neurobiology, 15, 437–443.

    Article  PubMed  CAS  Google Scholar 

  • Scheich, H., Bullock, T. H., & Hamstra, R. H. (1973). Coding properties of two classes of afferent nerve fibers: High frequency electroreceptors in the electric fish, Eigenmannia. Journal of Neurophysiology, 36, 39–60.

    PubMed  CAS  Google Scholar 

  • Selinger, J. V., Kulagina, N. V., O’Shaughnessy, T. J., Ma, W., & Pancrazio, J. J. (2007). Methods for characterizing interspike intervals and identifying bursts in neuronal activity. Journal of Neuroscience Methods, 162, 64–71.

    Article  PubMed  Google Scholar 

  • Strong, S. P., Koberle, R., de Ruyter van Steveninck, R. R., & Bialek, W. (1998). Entropy and information in neural spike trains. Physical Review Letters, 80, 197–200.

    Article  CAS  Google Scholar 

  • Takahashi, T., Moiseff, A., & Konishi, M. (1984). Time and Intensity cues are processed independently in the auditory system of the owl. Journal of Neuroscience, 4, 1781–1786.

    PubMed  CAS  Google Scholar 

  • von der Emde, G. (1990). Discrimination of objects through electrolocation in the weakly electric fish Gnathonemus petersii. Journal of Comparative Physiology A, 167, 413–422.

    Google Scholar 

  • von der Emde, G. (1998). Capacitance detection in the wave-type electric fish Eigenmannia during active electrolocation. Journal of Comparative Physiology A, 182, 217–224.

    Article  Google Scholar 

  • von der Emde, G. (1999). Active electrolocation of objects in weakly electric fish. Journal of Experimental Biology, 202, 1205–1215.

    PubMed  Google Scholar 

  • von der Emde, G., & Ringer, T. (1992). Electrolocation of capacitive objects in four species of pulse-type weakly electric fish. I. Discrimination performance. Ethology, 91, 326–338.

    Article  Google Scholar 

  • Wessel, R., Koch, C., & Gabbiani, F. (1996). Coding of time-varying electric field amplitude modulations in a wave-type electric fish. Journal of Neurophysiology, 75, 2280–2293.

    PubMed  CAS  Google Scholar 

  • Young, E. D. (1998). Parallel processing in the nervous system: Evidence from sensory maps. Proceedings of the National Academy of Sciences of the United States of America, 95, 933–934.

    Article  PubMed  CAS  Google Scholar 

  • Zakon, H. H. (1986). The electroreceptive periphery. In T. H. Bullock & W. Heiligenberg (Eds.), Electroreception (pp. 103–156). New York: John Wiley & Sons.

    Google Scholar 

Download references

Acknowledgements

We thank F. Gabbiani and A.M. Oswald for assistance with the feature extraction method. This work was supported by grants from the National Institute of Neurological Disorders and Stroke (F32 NS049788 to B.A.C.) and the National Science Foundation (IBN-0235533 to M.K.).

Author information

Author notes

  1. Bruce A. Carlson

    Present address: Department of Neurobiology & Behavior, Cornell University, Seeley G. Mudd Hall, Ithaca, NY, 14853, USA

Authors and Affiliations

  1. Department of Biology, University of Virginia, Charlottesville, VA, 22904, USA

    Bruce A. Carlson & Masashi Kawasaki

Authors
  1. Bruce A. Carlson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Masashi Kawasaki
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bruce A. Carlson.

Additional information

Action Editor: Matthew Wiener

Rights and permissions

Reprints and permissions

About this article

Cite this article

Carlson, B.A., Kawasaki, M. From stimulus estimation to combination sensitivity: encoding and processing of amplitude and timing information in parallel, convergent sensory pathways. J Comput Neurosci 25, 1–24 (2008). https://doi.org/10.1007/s10827-007-0062-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10827-007-0062-6

Keywords

Search

Navigation