Skip to main content
SpringerLink
Log in

Do Neocortical Pyramidal Neurons Display Stochastic Resonance?

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

Abstract

Neocortical pyramidal neurons in vivo are subject to an intense synaptic background activity that has a significant impact on various electrophysiological properties and dendritic integration. Using detailed biophysical models of a morphologically reconstructed neocortical pyramidal neuron, in which synaptic background activity was simulated according to recent measurements in cat parietal cortex in vivo, we show that the responsiveness of the cell to additional periodic subthreshold stimuli can be significantly enhanced through mechanisms similar to stochastic resonance. We compare several paradigms leading to stochastic resonance-like behavior, such as varying the strength or the correlation in the background activity. A new type of resonance-like behavior was obtained when the correlation was varied, in which case the responsiveness is sensitive to the statistics rather than the strength of the noise. We suggest that this type of resonance may be relevant to information processing in the cerebral cortex.

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

Similar content being viewed by others

References

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

    Google Scholar 

  • Benzi R, Suter A, Vulpiani A (1981) The mechanism of stochastic resonance. J. Phys. A14:L453-L457.

    Google Scholar 

  • Bezrukov SM, Vodyanoy I (1997) Stochastic resonance in nondynamical systems without response thresholds. Nature 385:319-321.

    Google Scholar 

  • Bulsara A, Jacobs EW, Zhou T, Moss F, Kiss L (1991) Stochastic resonance in a single neuron model: Theory and analog simulation. J. Theor. Biol. 152:531-555.

    Google Scholar 

  • Capurro A, Pakdaman K, Nomura T, Sato S (1998) Aperiodic stochastic resonance with correlated noise. Phys. Rev. E 58:4820-4827.

    Google Scholar 

  • Chialvo DR, Apkarian AV (1993) Modulated noisy biological dynamics: Three examples. J. Stat. Phys. 70:375-391.

    Google Scholar 

  • Chow CC, Imhoff TT, Collins JJ (1998) Enhancing aperiodic stochastic resonance through noise modulation. Chaos 8:616-620.

    Google Scholar 

  • Collins JJ, Chow CC, Imhoff TT (1995) Stochastic resonance without tuning. Nature 376:236-238.

    Google Scholar 

  • Collins JJ, Imhoff TT, Grigg P (1996) Noise enhanced information transmission in rat SA1 cutaneous mechanoreceptors via a periodic stochastic resonance. J. Neurophysiol. 76:642-645.

    Google Scholar 

  • Contreras D, Destexhe A, Steriade M (1997) Intracellular and computational characterization of the intracortical inhibitory control of synchronized thalamic inputs in vivo. J. Neurophysiol. 78:335-350.

    Google Scholar 

  • Contreras D, Timofeev I, Steriade M (1996) Mechanisms of long lasting hyperpolarizations underlying slow sleep oscillations in cat corticothalamic networks. J. Physiol. 494:251-264.

    Google Scholar 

  • Cook EP, Johnston D (1997) Active dendrites reduce location-dependent variability of synaptic input trains. J. Neurophysiol. 78:2116-2128.

    Google Scholar 

  • Cragg BG (1967) The density of synapses and neurons in the motor and visual areas of the cerebral cortex. J. Anat. 101:639-654.

    Google Scholar 

  • DeFelipe J, Fariñ as I (1992) The pyramidal neuron of the cerebral cortex: Morphological and chemical characteristics of the synaptic inputs. Prog. Neurobiol. 39:563-607.

    Google Scholar 

  • Denk W, Webb WW (1989) Thermal-noise-limited transduction observed in mechanosensory receptors of the inner ear. Phys. Rev. Lett. 63:207-210.

    Google Scholar 

  • Destexhe A, Mainen ZF, Sejnowski TJ (1998) Kinetic models of synaptic transmission. In: Koch C, Segev I, eds. Methods in Neuronal Modeling (2nd ed.). MIT Press, Cambridge, MA, pp. 1-26.

    Google Scholar 

  • Destexhe A (2001) Simplified models of neocortical pyramidal cells preserving somatodendritic voltage attenuation. Neurocomputing. 38:167-173.

    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.

    Google Scholar 

  • Douglas RJ, Wilkens L, Pantazelou E, Moss F (1993) Noise enhancement of information transfer in crayfish mechanoreceptors by stochastic resonance. Nature 365:337-340.

    Google Scholar 

  • Evarts EV (1964) Temporal patterns of discharge of pyramidal tract neurons during sleep and waking in the monkey. J. Neurophysiol. 27:152-171.

    Google Scholar 

  • Fauve S, Heslot FJ (1993) Stochastic resonance in a bistable system. Phys. Lett. A97:5-7.

    Google Scholar 

  • French CR, Sah P, Buckett KJ, Gage PW (1990) Avoltage-dependent persistent sodium current in mammalian hippocampal neurons. J. Gen. Physiol. 95:1139-1157.

    Google Scholar 

  • Gammaitoni L, Hänggi P, Jung P, Marchesoni F (1998) Stochastic resonance. Rev. Mod. Phys. 70:223-287.

    Google Scholar 

  • Gerstein GL, Bedenbaugh P, Aertsen AJ (1989) Neuronal assemblies. IEEE Trans. Biomed. Eng. 36:4-14.

    Google Scholar 

  • Gruner JE, Hirsch JC, Sotelo C (1974) Ultrastructural features of the isolated suprasylvian gyrus. J. Comp. Neurol. 154:1-27.

    Google Scholar 

  • Hines ML, Carnevale NT (1997) The NEURON simulation environment. Neural Computation 9:1179-1209.

    Google Scholar 

  • Hô N, Destexhe A (2000) Synaptic background activity enhances the responsiveness of neocortical pyramidal neurons. J. Neurophysiol. 84:1488-1496.

    Google Scholar 

  • Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117:500-544.

    Google Scholar 

  • Hubel D (1959) Single-unit activity in striate cortex of unrestrained cats. J. Physiol. 147:226-238.

    Google Scholar 

  • Huber MT, Krieg JC, Dewald M, Voigt K, Braun HA (1998) Stimulus sensitivity and neuromodulatory properties of noise intrinsic neuronal oscillators. BioSystems 48:95-104.

    Google Scholar 

  • Huguenard JR, Hamill OP, Prince DA (1988) Developmental changes in Na+ conductances in rat neocortical neurons: Appearance of a slow inactivating component. J. Neurophysiol. 59:778-795.

    Google Scholar 

  • Huguenard JR, McCormick DA (1992) Simulation of the currents involved in rhythmic oscillations in thalamic relay neurons. J. Neurophysiol. 68:1373-1383.

    Google Scholar 

  • Ivey C, Apkarian AV, Chivalvo DR (1998) Noise-induced tuning curve changes in mechanoreceptors. J. Neurophysiol. 79:1879-1890.

    Google Scholar 

  • Jaramillo F, Wiesenfeld K (1998) Mechanoelectrical transduction assisted by Brownian motion: A role for noise in the auditory system. Nature Neuroscience 1:384-388.

    Google Scholar 

  • Johnston D, Magee JC, Colbert CM, Cristie BR (1996) Active properties of neuronal dendrites. Annual Rev. Neurosci. 19:165-186.

    Google Scholar 

  • Lampl I, Reichova I, Ferster D (1999) Synchronous membrane potential fluctuations in neurons of the cat visual cortex. Neuron 22:361-374.

    Google Scholar 

  • Larkman AU (1991) Dendritic morphology of pyramidal neurons of the visual cortex of the rat. III. Spine distributions. J. Comp. Neurol. 306:332-343.

    Google Scholar 

  • Lee SG, Kim S (1999) Parameter dependence of stochastic resonance in the stochastic Hodgkin-Huxley neuron. Phys. Rev. E 60:826-830.

    Google Scholar 

  • Lee SG, Neiman A, Kim S (1998) Coherence resonance in a Hodgkin-Huxley neuron. Phys. Rev. E 57:3292-3297.

    Google Scholar 

  • Levin JE, Miller JP (1996) Broadband neural coding in the cricket sensory system enhanced by stochastic resonance. Nature 380:165-168.

    Google Scholar 

  • Longtin A (1993) Stochastic resonance in neuron models. J. Stat. Phys. 70:309-327.

    Google Scholar 

  • Longtin A, Bulsara A, Moss F (1991) Time-interval sequences in bistable systems and the noise-induced transmission of information by sensory neurons. Phys. Rev. Lett. 67:656-659.

    Google Scholar 

  • Longtin A, Chialvo DR (1998) Stochastic and deterministic resonance for excitable systems. Phys. Rev. Lett. 81:4012-4015.

    Google Scholar 

  • Lytton WW (1996) Optimizing synaptic conductance calculation for network simulations. Neural Computation 8:501-509.

    Google Scholar 

  • Magee JC, Johnston D (1995a) Characterization of single voltagegated sodium and calcium channels in the apical dendrites of rat CA1 pyramidal neurons. J. Physiol. 487:67-90.

    Google Scholar 

  • Magee JC, Johnston D (1995b) Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. Science 268:301-304.

    Google Scholar 

  • Mar DJ, Chow CC, Gerstner W, Adams RW, Collins JJ (1999) Noise shaping in populations of coupled model neurons. Proc. Natl. Acad. Sci. USA 96:10450-10455.

    Google Scholar 

  • Mato G (1998) Stochastic resonance in neural systems: Effects of temporal correlation in the spike trains. Phys. Rev. E 58:876-880.

    Google Scholar 

  • Matsumura M, Cope T, Fetz EE (1988) Sustained excitatory synaptic input to motor cortex neurons in awake animals revealed by intracellular recording of membrane potentials. Exp. Brain Res. 70:463-469.

    Google Scholar 

  • McCormick DA, Huguenard JR (1992) A model of the electrophysiological properties of thalamocortical relay neurons. J. Neurophysiol. 68:1384-1400.

    Google Scholar 

  • Migliore M, Hoffman DA, Magee JC, Johnston D (1999) Role of an A-type K+ conductance in the back-propagation of action potentials in the dendrites of hippocampal pyramidal neurons. J. Comp. Neurosci. 7:5-15.

    Google Scholar 

  • Neiman A, Pei X, Russell D, Wojtenek W, Wilkens L, Moss F, Braun HA, Huber MT, Voigt K (1999a) Synchronization of the noisy electrosensitive cells in the paddlefish. Phys. Rev. Lett. 82:660-663.

    Google Scholar 

  • Neiman A, Schimansky-Geier L, Moss F, Shulgin B, Collins JJ (1999b) Synchronization of noisy systems by stochastic signals. Phys. Rev. E 60:284-292.

    Google Scholar 

  • Nicolis C (1982) Stochastic aspects of climatic transitions: Response to a periodic forcing. Tellus 34:1.

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Pei X, Wilkens AL, Moss F (1996) Light enhances hydrodynamic signaling in the multimodal caudal photoreceptor interneurons of the crayfish. J. Neurophysiol. 76:3002-3011.

    Google Scholar 

  • Press WH, Teukolsky SA, Vetterling WT, Flannery BP (1993) Numerical Recipes in C: The Art of Scientific Computing. (2nd ed.). Cambridge University Press, Cambridge.

    Google Scholar 

  • Richardson KA, Imhoff TT, Grigg P, Collins JJ (1998) Using electrical noise to enhance the ability of humans to detect subthreshold mechanical cutaneous stimuli. Chaos 8:599-603.

    Google Scholar 

  • Rudolph M, Destexhe A (2000) Models of neocortical pyramidal neurons in the presence of correlated synaptic background activity: High discharge variability, enhanced responsiveness and independence of input location. Soc. Neurosci. Abstracts 26:1623.

    Google Scholar 

  • Segev I, Rall W (1998) Excitable dendrites and spines: Earlier theoretical insights elucidate recent direct observations. Trends Neurosci. 21:453-460.

    Google Scholar 

  • Shimokawa T, Rogel A, Pakdaman K, Sato S (1999) Stochastic resonance and spike-timing precision in an ensemble of leaky integrate and fire neuron models. Phys. Rev. E 59:3461-3470.

    Google Scholar 

  • Simonotto E, Riani M, Seife C, Roberts M, Twitty J, Moss F (1997) Visual perception of stochastic resonance. Phys. Rev. Lett. 78:1186-1189.

    Google Scholar 

  • Srebo R, Malladi P (1999) Stochastic resonance of the visually evoked potential. Phys. Rev. E 59:2566-2570.

    Google Scholar 

  • Stacey WC, Durand DM (2000) Stochastic resonance improves signal detection in hippocampal CA1 neurons. J. Neurophysiol. 83:1394-1402.

    Google Scholar 

  • Steriade M (1978) Cortical long-axoned cells and putative interneurons during the sleep-waking cycle. Behav. Brain Sci. 3:465-514.

    Google Scholar 

  • Steriade M, Timofeev I, Grenier F (2001) Natural waking and sleep states: A view from inside neocortical neurons. J. Neurophysiol. 85:1969-1985.

    Google Scholar 

  • Stuart GJ, Sakmann B (1994) Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367:69-72.

    Google Scholar 

  • Szentagothai J (1965) The use of degeneration in the investigation of short neuronal connections. In: Singer M, Shade JP, eds. Progress in Brain Research 14. Elsevier, Amsterdam. pp. 1-32.

    Google Scholar 

  • Traub RD, Miles R (1991) Neuronal Networks of the Hippocampus. Cambridge University Press, Cambridge.

    Google Scholar 

  • Wang W, Wang Y, Wang ZD (1998) Firing and signal transduction associated with an intrinsic oscillation in neuronal systems. Phys. Rev. E 57:R2527-R2530.

    Google Scholar 

  • White EL (1989) Cortical Circuits. Birkhauser, Boston.

    Google Scholar 

  • Wiesenfeld K, Moss F (1995) Stochastic resonance and the benefits of noise: From ice ages to crayfish and SQUIDS. Nature 373:33-36.

    Google Scholar 

  • Yamada WM, Koch C, Adams PR (1989) Multiple channels and calcium dynamics. In: Koch C, Segev I, eds. Methods in Neuronal Modeling. MIT Press, Cambridge, MA.

    Google Scholar 

  • Zhou T, Moss F (1990) Analog simulations of stochastic resonance. Phys. Rev. A41:4255-4264.

    Google Scholar 

  • Zohary E, Shadlen MN, Newsome WT (1994) Correlated neuronal discharge rate and its implications for psychophysical performance. Nature 370:140-143.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Unité de Neurosciences Intégratives et Computationnelles, CNRS, Bat. 33, Avenue de la Terrasse 1, 91198, Gif-sur-Yvette, France

    Michael Rudolph & Alain Destexhe

  2. Department of Physiology, Laval University, Québec, G1K 7P4, Canada

    Michael Rudolph & Alain Destexhe

Authors
  1. Michael Rudolph
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alain Destexhe
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rudolph, M., Destexhe, A. Do Neocortical Pyramidal Neurons Display Stochastic Resonance?. J Comput Neurosci 11, 19–42 (2001). https://doi.org/10.1023/A:1011200713411

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1011200713411

Search

Navigation