Skip to main content

Physiological Aspects of the Use of the Hodgkin–Huxley Model of Action Potential Generation for Neurons in Invertebrates and Vertebrates

Neuroscience and Behavioral Physiology volume 47, pages 751–757 (2017)Cite this article

Recent studies have shown that the dynamics of action potential generation in neurons in vertebrates, in contrast to invertebrates, is significantly different from the slow exponential dynamics predicted by the Hodgkin–Huxley equations and is characterized by a sudden kink-like origin in the form of a steep linear increase. In this context, new and important aspects of studies of the links between the dynamics of action potential generation and the frequency coding abilities of neurons and neuronal networks have been found. This review addresses contemporary models describing the kink-type dynamics of action potential generation, including an alternative model of cooperative activation of potential-dependent sodium channels and the effects of the dynamics of action potential generation on the processing abilities of neural networks. The relevance of this direction comes from the fact that despite the rapid development of neuron simulation in recent years, generally accepted models of nerve cells cannot provide a realistic description of the complete dynamics of action potential generation in mammalian neurons or correct assessments of the ability of these cells to encode high-frequency signals. Contemporary experimental and theoretical analyses of action potential generation and neuronal encoding, as summarized in the present work, are highly significant for improving our understanding of nerve cell physiology and assisting the creation of more accurate and correct models of neurons.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price includes VAT (USA)
Tax calculation will be finalised during checkout.

References

  • Baranauskas, G. and Martina, M., “Sodium currents activate without a Hodgkin-and-Huxley-type delay in central mammalian neurons,” J. Neurosci., 26, 671–684 (2006).

    CAS  Article  PubMed  Google Scholar 

  • Baranauskas, G., Mukovskiy, A., Wolf, F., and Volgushev, M., “The determinants of the onset dynamics of action potentials in a computational model,” Neuroscience, 167, 1070–1090 (2010).

    CAS  Article  PubMed  Google Scholar 

  • Boucsein, C., Tetzlaff, T., Meier, R., et al., “Dynamical response properties of neocortical neuron ensembles: Multiplicative versus additive noise,” J. Neurosci., 29, 1006–1010 (2009).

    CAS  Article  PubMed  Google Scholar 

  • Destexhe, A. and Pare, D., “Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo,” J. Neurophysiol., 81, 1531–1547 (1999).

    CAS  PubMed  Google Scholar 

  • Eyal, G., Mansvelder, H. D., de Kock, C. P. J., and Segev, I., “Dendrites impact the encoding capabilities of the axon,” J. Neuroscience, 34, No. 24, 8063–8071 (2014).

    CAS  Article  PubMed  Google Scholar 

  • Fleidervish, I. A., Lasser-Ross, N., Gutnick, M. J., and Ross, W. N., “Na+ imaging reveals little difference in action potential-evoked Na+ influx between axon and soma,” Nat. Neurosci., 13, No. 7, 852–60 (2010).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Fourcaud-Trocmé, N., Hansel, D., van Vreeswijk, C., and Brunei, N., “How spike generation mechanisms determine the neuronal response to fluctuating inputs,” J. Neurosci., 23, 11,628–11,640 (2003).

    Google Scholar 

  • Foust, A. J., Popovic, M., Zecevic, D., and McCormick, D. A., “Action potentials initiate in the axon initial segment and propagate through axon collaterals reliably in cerebellar Purkinje neurons,” J. Neurosci., 30, No. 20, 6891–6902 (2010).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Higgs, M. H. and Spain, W. J., “Conditional bursting enhances resonant firing in neocortical layer 2–3 pyramidal neurons,” J. Neurosci., 29, 1285–1299 (2009).

    CAS  Article  PubMed  Google Scholar 

  • Hille, B., Ion Channels of Excitable Membranes, Sinauer Assoc., Inc. Publ., Sunderland, MA, USA (2001).

  • Hodgkin, A. L. and Huxley, A. F., “Measurement of current-voltage relations in the membrane of the giant axon of Loligo,” J. Physiol., 116, 424–448 (1952a).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Hodgkin, A. L. and Huxley, A. F., “Currents carried by sodium and potassium ions through the membrane of the giant axon of Loligo,” J. Physiol., 116, 449–472 (1952b).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Hodgkin, A. L. and Huxley, A. F., “A quantitative description of membrane current and its application to conduction and excitation in nerve,” J. Physiol., 117, 500–544 (1952c).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Ilin, V., Malyshev, A., Wolf, E., and Volgushev, M., “Fast computations in cortical ensembles require rapid initiation of action potentials,” J. Neurosci., 33, No. 6, 2281–2292 (2013).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Jansen, R. F., Pieneman, A., and Ter Maat, A., “Spontaneous switching between ortho- and antidromic spiking as the normal mode of firing in the cerebral giant neurons of freely behaving Lymnaea stagnalis,” J. Neurophysiol., 76, No. 6, 4206–9 (1996).

    CAS  PubMed  Google Scholar 

  • Köndgen, H., Geisler, C., Fusi, S., et al., “The dynamical response properties of neocortical neurons to temporally modulated noisy inputs in vitro,” Cereb. Cortex, 18, 2086–2097 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  • Kole, M. H., Letzkus, J. J., and Stuart, G. J., “Axon initial segment Kv1 channels control axonal action potential waveform and synaptic efficacy,” Neuron, 55, No. 4, 633–47 (2007).

    CAS  Article  PubMed  Google Scholar 

  • Kole, M. H., Ilschner, S., Kampa, B. M., et al., “Action potential generation requires a high sodium channel density in the axon initial segment,” Nat. Neurosci., 11, No. 2, 178–86 (2008).

    CAS  Article  PubMed  Google Scholar 

  • Mainen, Z. F., Joerges, J., Huguenard, J. R., and Sejnowski, T. J., “A model of spike initiation in neocortical pyramidal neurons,” Neuron, 15, 1427–1439 (1995).

    CAS  Article  PubMed  Google Scholar 

  • Malyshev, A., Tchumatchenko, T., Volgushev, S., and Volgushev, M., “Energy-efficient encoding by shifting spikes in neocortical neurons,” Eur. J. Neurosci., 38, No. 8, 3181–8 (2013).

    Article  PubMed  Google Scholar 

  • McCormick, D. A., Shu, Y., and Yu, Y., “Neurophysiology: Hodgkin and Huxley model – still standing?” Nature, 445, E1-2, Discus. E2-3 (2007).

  • Naundorf, B., Geisel, T., and Wolf, F., “Action potential onset dynamics and the response speed of neuronal populations,” J. Comput. Neurosci., 18, 297–309 (2005).

    CAS  Article  PubMed  Google Scholar 

  • Naundorf, B., Wolf, F., and Volgushev, M., “Unique features of action potential initiation in cortical neurons,” Nature, 440, 1060–1063 (2006).

    CAS  Article  PubMed  Google Scholar 

  • Nikitin, E. S., Vavoulis, D., Kemenes, I., et al., “Persistent sodium current is a nonsynaptic substrate for long-term associative memory,” Curr. Biol., 18, 1221–6 (2008).

    CAS  Article  PubMed  Google Scholar 

  • Palmer, L. M. and Stuart, G. J., “Site of action potential initiation in layer 5 pyramidal neurons,” J. Neurosci., 26, No. 6, 1854–63 (2006).

    CAS  Article  PubMed  Google Scholar 

  • Patlak, J., “Molecular kinetics of voltage-dependent Na+ channels,” Physiol. Rev., 71, 1047–1080 (1991).

    CAS  PubMed  Google Scholar 

  • Popovic, M. A., Foust, A. J., McCormick, D. A., and Zecevic, D., “The spatio-temporal characteristics of action potential initiation in layer 5 pyramidal neurons: a voltage imaging study,” J. Physiol., 589, 4167–4187 (2011).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Shu, Y., Duque, A., Yuguo, Yu., et al., “Properties of action potential initiation in neocortical pyramidal cells: evidence from whole cell axon recordings,” J. Neurophysiol., 97, 746–760 (2007).

    Article  PubMed  Google Scholar 

  • Silberberg, G., Bethge, M., Markram, H., et al., “Dynamics of population rate codes in ensembles of neocortical neurons,” J. Neurophysiol., 91, 704–709 (2004).

    CAS  Article  PubMed  Google Scholar 

  • Stanford, T. R., Shankar, S., Massoglia, D. P., et al., “Perceptual decision making in less than 30 milliseconds,” Nat. Neurosci., 13, 379–385 (2010).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Tchumatchenko, T., Malyshev, A., Wolf, F., and Volgushev, M., “Ultrafast population encoding by cortical neurons,” J. Neurosci., 31, No. 34, 12171–12179 (2011).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  • Vavoulis, D. V., Nikitin, E. S., Kemenes, I., et al., “Balanced plasticity and stability of the electrical properties of a molluscan modulatory interneuron after classical conditioning: a computational study,” Front. Behav. Neurosci., 4, 19 (2010).

    PubMed  PubMed Central  Google Scholar 

  • Volgushev, M., Malyshev, A., Balaban, P., et al., “Onset dynamics of action potentials in rat neocortical neurons and identified snail neurons: quantification of the difference,” PLoS One, 3, No. 4, e1962 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, X. J., Lui, Y., Sanchez-Vives, M. V., and McCormick, D. A., “Adaptation and temporal decorrelation by single neurons in the primary visual cortex,” J. Neurophysiol., 89, 3279–3293 (2003).

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Moscow, Russia

    E. S. Nikitin, A. Yu. Malyshev, P. M. Balaban & M. A. Volgushev

Authors
  1. E. S. Nikitin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Yu. Malyshev
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. M. Balaban
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. A. Volgushev
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. S. Nikitin.

Additional information

Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 66, No. 3, p. 279–288, May–June, 2016.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Nikitin, E.S., Malyshev, A.Y., Balaban, P.M. et al. Physiological Aspects of the Use of the Hodgkin–Huxley Model of Action Potential Generation for Neurons in Invertebrates and Vertebrates. Neurosci Behav Physi 47, 751–757 (2017). https://doi.org/10.1007/s11055-017-0463-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11055-017-0463-6

Keywords

  • frequency encoding
  • action potentials
  • axons
  • action potential generation theory
  • action potential rise time