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 Biology  2004 

Amplification of Trial-to-Trial Response Variability by Neurons in Visual Cortex

DOI: 10.1371/journal.pbio.0020264

Full-Text   Cite this paper   Add to My Lib

Abstract:

The visual cortex responds to repeated presentations of the same stimulus with high variability. Because the firing mechanism is remarkably noiseless, the source of this variability is thought to lie in the membrane potential fluctuations that result from summated synaptic input. Here this hypothesis is tested through measurements of membrane potential during visual stimulation. Surprisingly, trial-to-trial variability of membrane potential is found to be low. The ratio of variance to mean is much lower for membrane potential than for firing rate. The high variability of firing rate is explained by the threshold present in the function that converts inputs into firing rates. Given an input with small, constant noise, this function produces a firing rate with a large variance that grows with the mean. This model is validated on responses recorded both intracellularly and extracellularly. In neurons of visual cortex, thus, a simple deterministic mechanism amplifies the low variability of summated synaptic inputs into the large variability of firing rate. The computational advantages provided by this amplification are not known.

References

[1]  Abeles M (1982) Role of the cortical neuron: Integrator or coincidence detector? Isr J Med Sci 18: 83–92.
[2]  Abeles M (1991) Corticonics: Neural circuits of the cerebral cortex. Cambridge, UK: Cambridge University Press. 280 p.
[3]  Amemori KI, Ishii S (2001) Gaussian process approach to spiking neurons for inhomogeneous Poisson inputs. Neural Comput 13: 2763–2797.
[4]  Anderson J, Carandini M, Ferster D (2000a) Orientation tuning of input conductance, excitation and inhibition in cat primary visual cortex. J Neurophysiol 84: 909–931.
[5]  Anderson JS, Lampl I, Gillespie DC, Ferster D (2000b) The contribution of noise to contrast invariance of orientation tuning in cat visual cortex. Science 290: 1968–1972.
[6]  Arieli A, Sterkin A, Grinvald A, Aertsen A (1996) Dynamics of ongoing activity: Explanation of the large variability in evoked cortical responses. Science 273: 1868–1871.
[7]  Azouz R, Gray CM (1999) Cellular mechanisms contributing to response variability of cortical neurons in vivo. J Neurosci 19: 2209–2223.
[8]  Bair W, Koch C (1996) Temporal precision of spike trains in extrastriate cortex of the behaving macaque monkey. Neural Comput 8: 1185–1202.
[9]  Boino D (2000) Modello delle risposte dei neuroni corticali in vitro [Laurea (thesis)]. Turin (Italy): University of Turin. 97 p.
[10]  Bonin V, Mante V, Carandini M (2003) Predicting signal and noise in LGN and V1. Program No. 229.5. In: Society for Neuroscience 2003 abstract viewer. Available: http://sfn.scholarone.com/itin2003/ via the Internet. Accessed 19 July 2004.
[11]  Bradley A, Scottun BC, Ohzawa I, Sclar G, Freeman RD (1987) Visual orientation and spatial frequency discrimination: A comparison of single cells and behavior. J Neurophysiol 57: 755–772.
[12]  Buracas GT, Zador AM, DeWeese MR, Albright TD (1998) Efficient discrimination of temporal patterns by motion-sensitive neurons in primate visual cortex. Neuron 20: 959–969.
[13]  Calvin WH, Stevens CF (1968) Synaptic noise and other sources of randomness in motoneuron interspike intervals. J Neurophysiol 31: 574–587.
[14]  Carandini M, Ferster D (2000) Membrane potential and firing rate in cat primary visual cortex. J Neurosci 20: 470–484.
[15]  Carandini M, Mechler F, Leonard CS, Movshon JA (1996) Spike train encoding in regular-spiking cells of the visual cortex. J Neurophysiol 76: 3425–3441.
[16]  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.
[17]  Freeman TCB, Durand S, Kiper DC, Carandini M (2002) Suppression without inhibition in visual cortex. Neuron 35: 759–771.
[18]  Geisler WS, Albrecht DG (1997) Visual cortex neurons in monkeys and cats: Detection, discrimination, and identification. Vis Neurosci 14: 897–919.
[19]  Granit R, Kernell D, Shortess GK (1963) Quantitative aspects of repetitive firing of mammalian motoneurons, caused by injected currents. J Physiol (Lond) 168: 911–931.
[20]  Gur M, Beylin A, Snodderly M (1997) Response variability of neurons in primary visual cortex (V1) of alert monkeys. J Neurosci 17: 2914–2920.
[21]  Hansel D, van Vreeswijk C (2002) How noise contributes to contrast invariance of orientation tuning in cat visual cortex. J Neurosci 22: 5118–5128.
[22]  Heeger DJ (1992) Half-squaring in responses of cat simple cells. Vis Neurosci 9: 427–443.
[23]  Heggelund P, Albus K (1978) Response variability and orientation discrimination of single cells in striate cortex of cat. Exp Brain Res 32: 197–211.
[24]  Jagadeesh B, Wheat HS, Ferster D (1993) Linearity of summation of synaptic potentials underlying direction selectivity in simple cells of the cat visual cortex. Science 262: 1901–1904.
[25]  Kara P, Reinagel P, Reid RC (2000) Low response variability in simultaneously recorded retinal, thalamic, and cortical neurons. Neuron 27: 635–646.
[26]  Kenet T, Bibitchkov D, Tsodyks M, Grinvald A, Arieli A (2003) Spontaneously emerging cortical representations of visual attributes. Nature 425: 954–956.
[27]  Lankheet MJ, Molenaar J, van de Grind WA (1989) The spike generating mechanism of cat retinal ganglion cells. Vision Res 29: 505–517.
[28]  Mainen ZF, Sejnowski TJ (1995) Reliability of spike timing in neocortical neurons. Science 268: 1503–1506.
[29]  Mechler F (1997) Neuronal response variability in the primary visual cortex [dissertation]. New York: New York University. 153 p.
[30]  Mechler F, Ringach DL (2002) On the classification of simple and complex cells. Vision Res 42: 1017–1033.
[31]  Miller KD, Troyer TW (2002) Neural noise can explain expansive, power-law nonlinearities in neural response functions. J Neurophysiol 87: 653–659.
[32]  Priebe NJ, Ferster D, Carandini M, Mechler F (2004) The spike threshold nonlinearity gives rise to the dichotomy between V1 simple and complex cells. Nat Neurosci. In press.
[33]  Reich DS, Victor JD, Knight BW, Ozaki T, Kaplan E (1997) Response variability and timing precision of neuronal spike trains in vivo. J Neurophysiol 77: 2836–2841.
[34]  Ress D, Heeger DJ (2003) Neuronal correlates of perception in early visual cortex. Nat Neurosci 6: 414–420.
[35]  Rice SO (1944) Mathematical analysis of random noise. AT&T Tech J 23: 282–332.
[36]  Rudolph M, Destexhe A (2003) Characterization of subthreshold voltage fluctuations in neuronal membranes. Neural Comput 15: 2577–2618.
[37]  Shadlen MN, Newsome WT (1998) The variable discharge of cortical neurons: Implications for connectivity, computation, and information coding. J Neurosci 18: 3870–3896.
[38]  Softky WR, Koch C (1993) The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J Neurosci 13: 334–350.
[39]  Stevens CF, Zador AM (1998) Input synchrony and the irregular firing of cortical neurons. Nat Neurosci 1: 210–217.
[40]  Svirskis G, Rinzel J (2000) Influence of temporal correlation of synaptic input on the rate and variability of firing in neurons. Biophys J 79: 629–637.
[41]  Tolhurst DJ, Movshon JA, Thompson ID (1981) The dependence of response amplitude and variance of cat visual cortical neurons on stimulus contrast. Exp Brain Res 41: 414–419.
[42]  Troyer TW, Miller KD (1997) Physiological gain leads to high ISI variability in a simple model of a cortical regular spiking cell. Neural Comput 9: 971–983.
[43]  Tsodyks M, Kenet T, Grinvald A, Arieli A (1999) Linking spontaneous activity of single cortical neurons and the underlying functional architecture. Science 286: 1943–1946.
[44]  Tuckwell HC (1988) Nonlinear and stochastic theories. Volume 2, Introduction to theoretical neurobiology. Cambridge (United Kingdom): Cambridge University Press. 288 p.
[45]  Vogels R, Spileers W, Orban GA (1989) The response variability of striate cortical neurons in the behaving monkey. Exp Brain Res 77: 432–436.
[46]  Volgushev M, Pernberg J, Eysel UT (2000) Comparison of the selectivity of postsynaptic potentials and spike responses in cat visual cortex. Eur J Neurosci 12: 257–263.
[47]  Volgushev M, Pernberg J, Eysel UT (2002) A novel mechanism of response selectivity of neurons in cat visual cortex. J Physiol 540: 307–320.
[48]  Wang XJ (1998) Calcium coding and adaptive temporal computation in cortical pyramidal neurons. J Neurophysiol 79: 1549–1566.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133