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Spike Generating Dynamics and the Conditions for Spike-Time Precision in Cortical Neurons

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Abstract

Temporal precision of spiking response in cortical neurons has been a subject of intense debate. Using a canonical model of spike generation, we explore the conditions for precise and reliable spike timing in the presence of Gaussian white noise. In agreement with previous results we find that constant stimuli lead to imprecise timing, while aperiodic stimuli yield precise spike timing. Under constant stimulus the neuron is a noise perturbed oscillator, the spike times follow renewal statistics and are imprecise. Under an aperiodic stimulus sequence, the neuron acts as a threshold element; the firing times are precisely determined by the dynamics of the stimulus. We further study the dependence of spike-time precision on the input stimulus frequency and find a non-linear tuning whose width can be related to the locking modes of the neuron. We conclude that viewing the neuron as a non-linear oscillator is the key for understanding spike-time precision.

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References

  • Adrian ED, Zotterman Y (1926) The impulses produced by sensory nerve endings. Part. 2. The response of a single end organ. J. Physiol. 61: 151-171.

    Google Scholar 

  • Azouz R, Gray CM (1999) Cellular mechanisms contributing to response variability of cortical neurons in vivo. J. Neuroscience 19: 2209-2223.

    Google Scholar 

  • Azouz R, Gray CM (2000) Dynamic spike threshold reveals a mechanism for synaptic coincidence detection in cortical neurons in vivo. Proc. Natl. Acad. Sci. USA 97: 8110-8115.

    Article  PubMed  Google Scholar 

  • Bair W, Koch C (1996) Temporal precision of spike trains in extrastriate cortex of the behaving macaque monkey. Neural Comp. 8: 1185-1202.

    Google Scholar 

  • Barlow H (1994) The neuron doctrine in perception. In: M Gazzaniga, ed. The Cognitive Neuroscience. MIT Press, Boston. pp. 415-435.

    Google Scholar 

  • Bialek W, Rieke F (1992) Reliability and information transmission in spiking neurons. Trends. Neurosci. 15: 428-434.

    Article  PubMed  Google Scholar 

  • Bishop PO, Levick WR, Williams WO (1964) Statistical analysis of the dark discharge of lateral geniculate neurones. J. Physiol. 170: 598-612.

    PubMed  Google Scholar 

  • Britten KH, Shadlen MN, Newsome WT, Movshon JA (1993) Response of neurons in macaque MT to stochastic motion signals. Visual Neurosci. 10: 1157-1169.

    Google Scholar 

  • Brunel N, Chance FS, Fourcard N, Abbott LF (2001) Effects of synaptic noise and filtering on the frequency response of spiking neurons. Phys. Rev. Lett. 86: 2186-2189.

    Article  PubMed  Google Scholar 

  • Bryant HL, Segundo JP (1976) Spike initiation by transmembrane current: A white-noise analysis. J. Physiol. 260: 279-314.

    PubMed  Google Scholar 

  • Bugmann G, Christodoulou C, Taylor JG (1997) Role of temporal integration and fluctuation detection in the highly irregular firing of a leaky integrator neuron model with partial reset. Neural Comp. 9: 985-1000.

    Google Scholar 

  • Calvin WH, Stevens CF (1968) Synaptic noise and other sources of randomness in motoneuron interspike intervals. J. Neurophysiol. 31: 574-587.

    PubMed  Google Scholar 

  • Connors BW, Gutnick MJ (1990) Intrinsic firing patterns of diverse neocortical neurons. Trends. Neurosci. 13: 99-104.

    Article  PubMed  Google Scholar 

  • Coombes S, Bressloff P (1999) Mode locking and Arnold tongues in integrate-and-fire neural oscillators. Phys. Rev. E 60: 2086-2096.

    Article  Google Scholar 

  • Cox DR (1970) Analysis of Binary Data. Chapman and Hall, London.

    Google Scholar 

  • de Charms RC, Zador A (2000) Neural representation and the cortical code. Annu. Rev. Neurosci. 23: 613-647.

    Article  PubMed  Google Scholar 

  • de Ruyter van Steveninck RR, Strong SP, Koberle R, Bialek W (1997) Reproducibility and variability in neural spike trains. Science 275: 1805-1808.

    Article  PubMed  Google Scholar 

  • Destexhe A, Paré D (1999) Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. J. Neurophysiol. 81: 1531-1547.

    PubMed  Google Scholar 

  • Destexhe A, Rudolph M, Fellous J-M, Sejnowski TJ (2001) Fluctuating synaptic conductances recreate in vivo-like activity in neocortical neurons. Neurosci. 107: 13-24.

    Article  Google Scholar 

  • Engel AK, König P, Kreiter AK, Schillen TB, Singer W (1992) Temporal coding in the visual cortex: New vistas on integration in the nervous system. Trends Neurosci. 15: 218-226.

    Article  PubMed  Google Scholar 

  • Ermentrout GB, Kopell NK (1984) Frequency plateaus in a chain of weakly coupled oscillators I. SIAM J. Math. Analysis 15: 215-237.

    Google Scholar 

  • Ermentrout GB, Kopell NK (1986) Parabolic bursting in an excitable system coupled with a slow oscillation. SIAM J. Appl. Math. 46: 233-253.

    Google Scholar 

  • Ermentrout GB, Pascal M, Gutkin B (2001) The effects of spike frequency adaptation and negative feedback on the synchronization of neural oscillators. Neural Comp. 13: 1285-1310.

    Article  Google Scholar 

  • Fellous J-M, Howeling AR, Modi RH, Rao RPN, Tiesinga PHE, Sejnowski T J (2000) Frequency dependence of spike timing reliability in cortical pyramidal cells and interneurons. J. Neurophys. 85: 1782-1787.

    Google Scholar 

  • Gray CM (2000) Synchronous oscillations in neuronal systems: Mechanisms and functions. J. Comp. Neurosci. 1: 11-38.

    Google Scholar 

  • Gutkin BS, Ermentrout GB (1998) Dynamics of membrane excitability determine interspike interval variability: A link between spike generation mechanisms and cortical spike train statistics. Neural Comp. 10: 1047-1065.

    Article  Google Scholar 

  • Gutkin BS, Laing C, Colby C, Chow CC, Ermentrout GB (2001) Turning on and off with excitation: The role of spike-timing synchrony and asynchrony in sustained neural activity. J. Comp. Neurosci. 11: 121-134.

    Article  Google Scholar 

  • Hansel D, Mato G, Meunier C (1995) Synchrony in excitatory neural networks. Neural Comp. 7: 307-337.

    Google Scholar 

  • Harsch A, Robinson HPC (2000) Postsynaptic variability of firing in rat cortical neurons: The role of input synchronization and synaptic NMDA receptor conductance. J. Neurosci. 20: 6181-6192.

    PubMed  Google Scholar 

  • Hodgkin AL (1948) The local changes associated with repetitive action in non-medulated axon. J. Physiol. 107: 165-181.

    Google Scholar 

  • Hoppensteadt F, Izhikevich E (1997) Weakly Connected Neural Nets. Springer-Verlag, Berlin.

    Google Scholar 

  • Howeling AR, Modi RH, Granter P, Fellous J-M, Sejnowski TJ (2001) Models of frequency preferences of prefrontal cortical neurons. Neurocomputing 38: 231-238.

    Article  Google Scholar 

  • Hunter JD, Milton JG, Thomas PJ, Cowan JD (1998) Resonance effect for neural spike time reliability. J. Neurophysiol. 80: 1427-1438.

    PubMed  Google Scholar 

  • Jensen R, Jones L, Gartner DH (1998) Synchronization of randomly driven nonlinear oscillators and the reliable firing of cortical neurons. In: JM Bower, ed. Computational Neuroscience: Trends in Research 1998. New York: Plenum.

    Google Scholar 

  • Kretzberg J, Egelhaaf M, Warzecha AK (2001) Membrane potential fluctuations determine the precision of spike timing and asynchronous activity: A model study. J. Comp. Neurosci. 10: 79-97.

    Article  Google Scholar 

  • Krüger J, Becker JD (1991) Recognizing the visual stimulus from neuronal discharges. Trends Neurosci. 14: 282-286.

    Article  PubMed  Google Scholar 

  • Latham PE, Richmond BJ, Nelson PG, Nirenberg S (2000) Intrinsic dynamics in neuronal networks. I. Theory. J. Neurophysiol. 83: 808-827.

    PubMed  Google Scholar 

  • MacKay D, McCulloch W (1952) The limiting information capacity of a neuronal link. Bull. Math. Biophys. 14: 127-135.

    Google Scholar 

  • Mainen ZF, Sejnowski T J (1995) Reliability of spike timing in neocortical neurons. Science 268: 1503-1506.

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • McCormick DA, Connors BW, Lighthall JW, Prince DA (1985) Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J. Neurophysiol. 54: 782-806.

    PubMed  Google Scholar 

  • Needleman DJ, Tisienga PHE, Sejnowski TJ (2001) Collective enhancement of precision in networks of coupled oscillators. Physica D 155: 324-336.

    Google Scholar 

  • Nowak LG, Sanchaez-Vives MV, McCormick DA (1997) Influence of low and high frequency inputs on spike timing in visual cortical neurons. Cerebral Cortex 7: 487-501.

    Article  PubMed  Google Scholar 

  • Panzeri S, Petersen RS, Schultz SR, Lebedev M, Diamond ME (2001) The role of spike timing in the coding of stimulus location in rat somatosensory cortex. Neuron 29: 769-777.

    Article  PubMed  Google Scholar 

  • Paré D, Shrink E, Gaudreau H, Destexhe A, Lang EJ (1998) Impact of spontaneous synaptic activity on the resting properties of cat neocortical pyramidal neurons in vivo. J. Neurophysiol. 79: 1450-1460.

    PubMed  Google Scholar 

  • Prut Y, Vaadia E, Bergman H, Haalman I, Slovin H, Abeles M (1998) Spatiotemporal structure of cortical activity: Properties and behavioral relevance. J. Neurophysiol. 79: 2857-2874.

    PubMed  Google Scholar 

  • Reinagel P, Reid RC (2000) Temporal coding of visual information in the thalamus. J Neurosci. 20: 5392-5400.

    PubMed  Google Scholar 

  • Rinzel JM, Ermentrout GB (1998) Analysis of Neuronal Excitability, in Methods in Neuronal Modeling, 2nd edn. C Koch, I Segev, eds. MIT Press Cambridge, MA.

    Google Scholar 

  • Rudolph M, Destexhe A (2002) Gain modulation and frequency locking under conductance noise. CNS 2002 Abstract.

  • Salinas E, Sejnowski TJ (2000) Impact of correlated synaptic input on output firing rate and variability in simple neuronal models. J. Neurosci. 20: 6193-6209.

    PubMed  Google Scholar 

  • Shadlen M, Newsome WT (1998) The variable discharge of cortical neurons: Implications for connectivity, computation, and information coding. J. Neurosci. 18: 3870-3896.

    PubMed  Google Scholar 

  • Stafstrom CE, Schwindt PC, Crill WE (1984) Repetitive fring in layer V neurons from cat neocortex in vitro. J. Neurophysiol. 52: 264-277.

    PubMed  Google Scholar 

  • Tang A (1997) Effects of cholinergic modulation on responses of neocortical neurons to fluctuating input. Cereb. Cortex 7: 502-509.

    Article  PubMed  Google Scholar 

  • Teich MC, Henegan C, Lowen SB, Ozaki T, Kaplan E (1997) Fractal character of the neural spike train in the visual system of the cat. J. Opt. Soc. Am. 14: 529-546.

    Google Scholar 

  • Theunissen F, Miller JP (1995) Temporal encoding in nervous systems: A rigorous definition. J. Comp. Neurosci. 2: 149-162.

    Google Scholar 

  • Thorpe S, Fize D, Marlot C (1996) Speed of processing in the human visual system. Nature 381: 520-522.

    Article  PubMed  Google Scholar 

  • Tovée MJ, Rolls ET, Treves A, Bellis RP (1993) Information encoding and the responses of single neurons in the primate temporal visual cortex. J. Neurophysiol. 70: 640-654.

    PubMed  Google Scholar 

  • Van Rossum MCW (2001) The transient precision of integrate and fire neurons: Effects of background activity and noise. J. Comp. Neurosci. 10: 303-311.

    Article  Google Scholar 

  • Wang X-J (1998) Calcium coding and adaptive temporal computation in cortical pyramidal neurons. J. Neurophysiol. 79: 1549-1566.

    PubMed  Google Scholar 

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Gutkin, B., Ermentrout, G.B. & Rudolph, M. Spike Generating Dynamics and the Conditions for Spike-Time Precision in Cortical Neurons. J Comput Neurosci 15, 91–103 (2003). https://doi.org/10.1023/A:1024426903582

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