全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2012 

Information Transmission in Cercal Giant Interneurons Is Unaffected by Axonal Conduction Noise

DOI: 10.1371/journal.pone.0030115

Full-Text   Cite this paper   Add to My Lib

Abstract:

What are the fundamental constraints on the precision and accuracy with which nervous systems can process information? One constraint must reflect the intrinsic “noisiness” of the mechanisms that transmit information between nerve cells. Most neurons transmit information through the probabilistic generation and propagation of spikes along axons, and recent modeling studies suggest that noise from spike propagation might pose a significant constraint on the rate at which information could be transmitted between neurons. However, the magnitude and functional significance of this noise source in actual cells remains poorly understood. We measured variability in conduction time along the axons of identified neurons in the cercal sensory system of the cricket Acheta domesticus, and used information theory to calculate the effects of this variability on sensory coding. We found that the variability in spike propagation speed is not large enough to constrain the accuracy of neural encoding in this system.

References

[1]  Shannon CE (1948) A mathematical theory of communication Bell Syst. Tech J 27: 379–423.
[2]  MacKay DM, McCulloch WS (1952) The limiting information capacity of a neuronal link. Bulletin of Mathematical Biology 14: 127–135.
[3]  Bialek W, Rieke F, de Ruyter van Steveninck RR, Warland D (1991) Reading a neural code. Science 252: 1854–1857.
[4]  de Ruyter van Steveninck RR, Lewen GD, Strong SP, Koberle R, Bialek W (1997) Reproducibility and variability in neural spike trains. Science 275: 1805–1808.
[5]  Gotch F (1910) The delay of the electrical response of nerve to a second stimulus. J Physiol 40: 250–274.
[6]  Adrian ED, Lucas K (1912) On the summation of propagated disturbances in nerve and muscle. J Physiol 44: 68–124.
[7]  Gasser HS, Erlanger J (1925) The nature of conduction of an impulse in the relatively refractory period. American Journal of Physiology 73: 613.
[8]  Bullock TH (1951) Facilitation of conduction rate in nerve fibers. J Physiol 114: 89–97.
[9]  Lass Y, Abeles M (1975) Transmission of information by the axon. I. Noise and memory in the myelinated nerve fiber of the frog. Biol Cybern 19: 61–67.
[10]  Bryant HL, Segundo JP (1976) Spike initiation by transmembrane current: a white-noise analysis. J Physiol 260: 279–314.
[11]  Miller RN, Rinzel J (1981) The dependence of impulse propagation speed on firing frequency, dispersion, for the Hodgkin-Huxley model. Biophys J 34: 227–259.
[12]  Musha T, Kosugi Y, Matsumoto G, Suzuki M (1981) Modulation of the time relation of action potential impulses propagating along an axon. IEEE Trans Biomed Eng 28: 616–623.
[13]  Borg J (1983) Effects of prior activity on the conduction in single motor units in man. J Neurol Neurosurg Psychiatry 46: 317–321.
[14]  Bowe CM, Kocsis JD, Waxman SG (1987) The association of the supernormal period and the depolarizing afterpotential in myelinated frog and rat sciatic nerve. Neuroscience 21: 585–593.
[15]  Horikawa Y (1991) Noise effects on spike propagation in the stochastic Hodgkin-Huxley models. Biol Cybern 66: 19–25.
[16]  Horikawa Y (1992) Spike propagation during the refractory period in the stochastic Hodgkin-Huxley model. Biological Cybernetics.
[17]  Debanne D (2004) Information processing in the axon. Nat Rev Neurosci 5: 304–316.
[18]  Monsivais P, Clark BA, Roth A, Hausser M (2005) Determinants of action potential propagation in cerebellar Purkinje cell axons. J Neurosci 25: 464–472.
[19]  Faisal AA, Laughlin SB (2007) Stochastic simulations on the reliability of action potential propagation in thin axons. PLoS Comput Biol 3: e79.
[20]  Baba Y, Hirota K, Yamaguchi T (1991) Morphology and response properties of wind-sensitive non-giant interneurons in the terminal abdominal ganglion of crickets. Zoolog Sci 8: 437–445.
[21]  Edwards JS, Palka J (1974) The cerci and abdominal giant fibres of the house cricket, Acheta domesticus. I. Anatomy and physiology of normal adults. Proc R Soc Lond B Biol Sci 185: 83–103.
[22]  Jacobs GA, Murphey RK (1987) Segmental origins of the cricket giant interneuron system. J Comp Neurol 265: 145–157.
[23]  Mendenhall B, Murphey RK (1974) The morphology of cricket giant interneurons. J Neurobiol 5: 565–580.
[24]  O'Shea M, Adams ME (1981) Pentapeptide (proctolin) associated with an identified neuron. Science 213: 567–569.
[25]  Hirota K, Sonoda Y, Baba Y, Yamaguchi T (1993) Distinction in morphology and behavioral role between dorsal and ventral groups of cricket giant interneurons. Zoolog Sci 10: 705–709.
[26]  Dimitrov AG, Miller JP, Gedeon T, Aldworth Z, Parker AE (2003) Analysis of neural coding through quantization with an information-based distortion measure. Network 14: 151–176.
[27]  Aldworth ZN, Miller JP, Gedeon T, Cummins GI, Dimitrov AG (2005) Dejittered spike-conditioned stimulus waveforms yield improved estimates of neuronal feature selectivity and spike-timing precision of sensory interneurons. J Neurosci 25: 5323–5332.
[28]  Aldworth ZN, Dimitrov AG, Cummins GI, Gedeon T, Miller JP (2011) Temporal Encoding in a Nervous System. PLoS Comput Biol 7: e1002041.
[29]  Kennel MB, Shlens J, Abarbanel HDI, Chichilnisky EJ (2005) Estimating entropy rates with bayesian confidence intervals. Neural Comput 17: 1531–1576.
[30]  Shlens J, Kennel MB, Abarbanel HDI, Chichilnisky EJ (2007) Estimating Information Rates with Confidence Intervals in Neural Spike Trains. Neural Comput 19: 1683–1719.
[31]  Goldberg DH, Victor JD, Gardner EP, Gardner D (2009) Spike train analysis toolkit: enabling wider application of information-theoretic techniques to neurophysiology. Neuroinformatics 7: 165–178.
[32]  Abeles M, Lass Y (1975) Transmission of information by the axon. II. The channel capacity. Biol Cybern 19: 121–125.
[33]  George SA (1977) Changes in interspike interval during propagation: quantitative description. Biol Cybern 26: 209–213.
[34]  Mainen ZF, Sejnowski TJ (1995) Reliability of spike timing in neocortical neurons. Science 268: 1503–1506.
[35]  Gabbiani F, Metzner W, Wessel R, Koch C (1996) From stimulus encoding to feature extraction in weakly electric fish. Nature 384: 564–567.
[36]  Oswald AM, Chacron MJ, Doiron B, Bastian J, Maler L (2004) Parallel processing of sensory input by bursts and isolated spikes. J Neurosci 24: 4351–4362.
[37]  Eyherabide HG, Rokem A, Herz AV, Samengo I (2008) Burst Firing is a Neural Code in an Insect Auditory System. Front Comput Neurosci 2: 3.
[38]  Dicaprio RA, Billimoria CP, Ludwar BC (2007) Information rate and spike-timing precision of proprioceptive afferents. J Neurophysiol 98: 1706–1717.
[39]  Kuriscak E, Trojan S, Wunsch Z (2002) Model of spike propagation reliability along the myelinated axon corrupted by axonal intrinsic noise sources. Physiol Res 51: 205–215.
[40]  Bucher D, Goaillard JM (2011) Beyond faithful conduction: Short-term dynamics, neuromodulation, and long-term regulation of spike propagation in the axon. Prog Neurobiol 94: 307–346.
[41]  Ballo AW, Bucher D (2009) Complex intrinsic membrane properties and dopamine shape spiking activity in a motor axon. J Neurosci 29: 5062–5074.
[42]  Kocsis JD, Malenka RC, Waxman SG (1983) Effects of extracellular potassium concentration on the excitability of the parallel fibres of the rat cerebellum. J Physiol 334: 225–244.
[43]  Roddey JC, Girish B, Miller JP (2000) Assessing the performance of neural encoding models in the presence of noise. J Comput Neurosci 8: 95–112.
[44]  Levin JE, Miller JP (1996) Broadband neural encoding in the cricket cercal sensory system enhanced by stochastic resonance. Nature 380: 165–168.
[45]  Weidner C, Schmelz M, Schmidt R, Hammarberg B, Orstavik K, et al. (2002) Neural signal processing: the underestimated contribution of peripheral human C-fibers. J Neurosci 22: 6704–6712.
[46]  Kohstall-Schnell D, Gras H (1994) Activity of giant interneurones and other wind-sensitive elements of the terminal ganglion in the walking cricket. J Exp Biol 193: 157–181.
[47]  Vedenina VY, Rozhkova GI, Panjutin AK, Byzov AL, K?mper G (1998) Frequency-intensity characteristics of cricket cercal interneurons: low-frequency-sensitive units. J Comp Physiol [A] 183: 553–561.
[48]  Jacobs GA, Miller JP, Aldworth Z (2008) Computational mechanisms of mechanosensory processing in the cricket. J Exp Biol 211: 1819–1828.
[49]  Abbott LF, Nelson SB (2000) Synaptic plasticity: taming the beast. Nat Neurosci. 3. pp. 1178–1183.
[50]  Sjostrom PJ, Turrigiano GG, Nelson SB (2001) Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron 32: 1149–1164.
[51]  Caporale N, Dan Y (2008) Spike timing-dependent plasticity: a Hebbian learning rule. Annu Rev Neurosci 31: 25–46.
[52]  Izhikevich EM, Desai NS, Walcott EC, Hoppensteadt FC (2003) Bursts as a unit of neural information: selective communication via resonance. Trends Neurosci 26: 161–167.
[53]  Ritzmann RE, Camhi JM (1978) Excitation of Leg motor neurons by giant interneurons in the cockroach Periplaneta americana. J Comp Physiol [A] 125: 305–316.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133