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Spatiotemporal burst coding for extracting features of spatiotemporally varying stimuli

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Abstract

Encoding features of spatiotemporally varying stimuli is quite important for understanding the neural mechanisms of various sensory coding. Temporal coding can encode features of time-varying stimulus, and population coding with temporal coding is adequate for encoding spatiotemporal correlation of stimulus features into spatiotemporal activity of neurons. However, little is known about how spatiotemporal features of stimulus are encoded by spatiotemporal property of neural activity. To address this issue, we propose here a population coding with burst spikes, called here spatiotemporal burst (STB) coding. In STB coding, the temporal variation of stimuli is encoded by the precise onset timing of burst spike, and the spatiotemporal correlation of stimuli is emphasized by one specific aspect of burst firing, or spike packet followed by silent interval. To show concretely the role of STB coding, we study the electrosensory system of a weakly electric fish. Weakly electric fish must perceive the information about an object nearby by analyzing spatiotemporal modulations of electric field around it. On the basis of well-characterized circuitry, we constructed a neural network model of the electrosensory system. Here we show that STB coding encodes well the information of object distance and size by extracting the spatiotemporal correlation of the distorted electric field. The burst activity of electrosensory neurons is also affected by feedback signals through synaptic plasticity. We show that the control of burst activity caused by the synaptic plasticity leads to extracting the stimulus features depending on the stimulus context. Our results suggest that sensory systems use burst spikes as a unit of sensory coding in order to extract spatiotemporal features of stimuli from spatially distributed stimuli.

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References

  • Arabzadeh E, Zorzin E, Diamond ME (2005) Neural encoding of texture in the whisker sensory pathway. PLos Bio 3:E17

    Google Scholar 

  • Assad C, Rasnow B, Stoddard PK (1999) Electric organ discharges and electric images during electrolocation. J Exp Biol 202:1185–1193

    PubMed  CAS  Google Scholar 

  • Bastian J (1981a) Electroreception I. How the electrorecetors of Apteronotus Leptorynchus code for moving objects and other electric stimuli? J Comp Physiol A 144:465–479

    Article  Google Scholar 

  • Bastian J (1981b) Electroreception II. The effects of moving objets and other electrical stimulli on the activities of two categories of posterior lateral line lobe cells in Apteronotus Albiforms. J Comp Physiol A 144:481–494

    Article  Google Scholar 

  • Bastian J (1986) In: Bullock TH, Heiligenberg W (eds) Electrorecption. Wiely, New York, pp 577–612

  • Bastian J (1991) Electrolocation. In: Arbib M (ed) The handbook of brain theory and neural network. MIT Press, Cambridge, pp 352–356

    Google Scholar 

  • Bastian J (1998) Plasticity in an electrosensory system III, contrasting properties of spatially segrefated dendriti inpputs. J Neurophysiol 79:1839–1857

    PubMed  CAS  Google Scholar 

  • Bastian J, Nguyenkim J (2001) Dendritic modulation of burst-like firing in sensory neurons. J Neurophysiol 85:10–22

    PubMed  CAS  Google Scholar 

  • Bastian J, Chacron MJ, Maler L (2004) Plastic and nonplastic pyramidal cell perform unique roles in a network capable of adaptive redundancy reduction. Neuron 41:767–779

    Article  PubMed  CAS  Google Scholar 

  • Bell CC, Bodzhick D, Montogomery J, Bastian J (1997a) The generation and substraction of sensory excitations within cerebellum-like structures. Brain Behav Evol 50:17–31

    PubMed  Google Scholar 

  • Bell CC, Han V, Sugawara Y, Grant K (1997b) Synaptic plasticity in a cerebellum-like structure depends on temporal order. Nature 387:278–281

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Doiron B, Laing C, Longtin A, Maler L (2002) Ghostbursing: a novel neuronal burst mechanism. J Comp Neurosci 12:5–25

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Doiron B, Oswald A-MM, Maler L (2007) Interval coding II. Dendritic dependent mechanisms. J Neurophysiol 97:2744–2757

    Article  PubMed  Google Scholar 

  • Fujita K, Kashimori Y (2006) Population coding of electrosensory stimulus in receptor network. Neurocomputing 69:1206–1210

    Article  Google Scholar 

  • Gehr DD, Komiya H, Eggermont JJ (2000) Neural responses in cat primary auditory cortex to natural and altered species-specific calls. Hear Res 150:27–42

    Article  PubMed  CAS  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 

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

    Google Scholar 

  • Hoshimiya N, Shogen K, Mastuo T, Chichibu S (1980) The Apteronotus EOD field: waveform and EOD field simulation. J Comp Physiol 135:283–290

    Article  Google Scholar 

  • Izhickvich EM, Desai NS, Walcott EC, Hoppersteadt FC (2003) Bursts as a unit of neural information: selective communication via resonance. Trends Neurosci 26:161–167

    Article  Google Scholar 

  • Jones LM, Depireux DA, Simons DJ, Keller A (2004) Robust temporal coding in the trigeminal system. Science 304:1986–1989

    Article  PubMed  CAS  Google Scholar 

  • Kashimori Y, Goto M, Kambara T (1996) A model of P- and T-electroreceptor of weakly electric fish. Biophys J 70:2513–2526

    Article  PubMed  CAS  Google Scholar 

  • Kashimori Y, Minagawa M, Inoue S, Hoshino O, Kambara T (2001) A neural model of electrosensory system making electrolocation of weakly electric fish. Neurocomputing 38-40:1349–1357

    Article  Google Scholar 

  • Krahe B, Gabbiani F (2004) Burst firing in sensory systems. Nat Rev Neurosci 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 neuron. J Neurosci 22:2374–2382

    PubMed  CAS  Google Scholar 

  • Laurent G (1999) A systems perspective on early olfactory coding. Science 286:723–728

    Article  PubMed  CAS  Google Scholar 

  • Laurent G, MacLeold K, Wehr M (1998) Spatiotemporal structure of olfactory inputs to the mushroom bodies. Learn Mem 5:124–132

    PubMed  CAS  Google Scholar 

  • Lemon N, Turner RW (2000) Conditional spike backpropagetion generates burst discharge in a sensory neuron. J Neurophysiol 84:1519–1530

    PubMed  CAS  Google Scholar 

  • Lewis JE, Maler L (2001) Neural population codes and the perception of object distance in weakly electric fish. J Neurosci 21:2842–2850

    PubMed  CAS  Google Scholar 

  • Lewis JE, Maler L (2002) Dynamics of electrosensory feedback: short-term plasticity and inhibition in a parallel fiber pathway. J Neurophysiol 88:1695–1706

    PubMed  Google Scholar 

  • Lewis JE, Maler L (2004) Synaptic dynamics on different time scales in a parallel fiber feedback pathway of the weakly electric fish. J Neurophysiol 91:1064–1070

    Article  PubMed  Google Scholar 

  • Lisman J (1997) Bursts as a unit of neural information:making unreliable synapses reliable. Trends Neurosci 20:38–43

    Article  PubMed  CAS  Google Scholar 

  • Maclurkin JW, Optican LM, Richmond BJ, Gawne TJ (1991) Concurrent processing and complexity of temporally encoded neuronal messages in visual perception. Science 253:675–677

    Article  Google Scholar 

  • Maler L, Sas E, Carr C, Matsubara J (1982) Efferent projections of the posterior lateral line lobe in a gymnotiform fish. J Comp Neurol 21:154–164

    Article  Google Scholar 

  • Malinow R, Otmakhov N, Blum KI, Lisman J (1994) Visualization hippocampal synaptic function by optical detection of Ca2+ entry through the N-methyl- D-aspartate channel. Proc Natl Acad Sci USA 91:8170–8174

    Article  PubMed  CAS  Google Scholar 

  • Masuda N, Doiron B, Logntin A, Aihara K (2005) Coding of temporaly varying signals in networks of spiking neurons with global delayed feedback. Neural Comput 17:2139–2175

    Article  PubMed  Google Scholar 

  • Mehaffey NW, Doiron B, Maler L, Turner R (2005) Deperministic multiplicative gain control with active dendrites. J Neurosci 25:9968–9977

    Article  PubMed  CAS  Google Scholar 

  • Meister M (1996) Mutineural codes in retinal signaling. Proc Natl Acad Sci USA 93:609–614

    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. J Neurosci 18:2283–2300

    PubMed  CAS  Google Scholar 

  • Nagarajan SS, Cheung SW, Bedenbaugh P, Beitel RE, Schreiner CE, Merzenich MM (2002) Representation of spectral and temporal envelope of twitter vocalization in common marmoset primary auditory cortex. J Neurophysiol 87: 1723–1737

    PubMed  Google Scholar 

  • Nelson ME, Xu Z, Payne JR (1997) Characterization and modeling of P-type electrosensory afferent responses to amplitude modulations in a wave-type electric fish. J Comp Physiol A 181:532–544

    Article  PubMed  CAS  Google Scholar 

  • Oswald A-MM, Lewis JE, Maler L (2001) Dynamically interacting processes underlie synaptic plasticity in a feedback pathway. J Neurophysiol 87:2450–2463

    Google Scholar 

  • Oswald A-MM, Doiron B, Maler L (2007) Interval coding I. Burst interspike intervals as indicators of stimulus intensity. J Neurophysiol 97:2731–2743

    Google Scholar 

  • Rasnow B (1996) The effects of simple objects on the electric field of Apteronotus. J Comp Physiol A 178:397–411

    Google Scholar 

  • Sherman SM (2001) Tonic and burst firing: dual modes of thalamocortical relay. Trends Neurosci 24:122–126

    Article  PubMed  CAS  Google Scholar 

  • Turner RW, Maler L, Deerinck T, Levinson SR (1994) Ellisman MH, TTX-sensitive dendritic sodium channels underlie oscillatory discharge in a verterbrate sensory neurons. J Neurosci 14:6453–6471

    PubMed  CAS  Google Scholar 

  • Von der Emde G, Schwarz S, Gomez L, Budelli R, Grant K (1998) Electric fish measure distance in the dark. Nature 395:890–894

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Kazuhisa Fujita.

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Fujita, K., Kashimori, Y. & Kambara, T. Spatiotemporal burst coding for extracting features of spatiotemporally varying stimuli. Biol Cybern 97, 293–305 (2007). https://doi.org/10.1007/s00422-007-0175-z

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  • DOI: https://doi.org/10.1007/s00422-007-0175-z

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