Biophysical basis for three distinct dynamical mechanisms of action potential initiation

PLoS Computational Biology

Volumn 4, Issue 10, 2008, Pages

  Prescott, Steven A ^a,b   De Koninck, Yves ^c   Sejnowski, Terrence J ^a,b,d  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c CENTRE DE RECHERCHE DE L INSTITUT UNIVERSITAIRE EN SANTÉ MENTALE DE QUÉBEC   (Canada)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOPHAGES; BIOPHYSICS; CHEMICAL ACTIVATION; ELECTROPHYSIOLOGY; HOPF BIFURCATION; SENSORY ANALYSIS;

'CURRENT; ACTION POTENTIAL INITIATIONS; ACTION-POTENTIALS; DYNAMICAL MECHANISMS; MECHANISM OF ACTION; POTENTIAL SPIKE; PROPERTY; STEADY STATE; SUBTHRESHOLD CURRENT; SYNAPTIC INPUT;

NEURONS;

ARTICLE; CONTROLLED STUDY; MALE; NERVE CELL EXCITABILITY; NERVE CELL STIMULATION; NONHUMAN; RAT; REED STERNBERG CELL; SENSORY NERVE CELL; SENSORY STIMULATION; SIGNAL TRANSDUCTION; SPINAL CORD NERVE CELL; ACTION POTENTIAL; ANIMAL; BIOLOGICAL MODEL; BIOLOGY; BIOPHYSICS; CLASSIFICATION; CYTOLOGY; ELECTROPHYSIOLOGY; IN VITRO STUDY; PHYSIOLOGY; SPINAL NERVE; SPRAGUE DAWLEY RAT;

ACTION POTENTIALS; ANIMALS; BIOPHYSICS; COMPUTATIONAL BIOLOGY; ELECTROPHYSIOLOGY; MALE; MODELS, NEUROLOGICAL; NEURONS, AFFERENT; RATS; RATS, SPRAGUE-DAWLEY; SPINAL NERVES;

EID: 55449122549     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1000198     Document Type: Article

References (55)

1. Adrian ED (1932) The Mechanism of Nervous Action: Electrical Studies of the Neurone. Philadelphia: University of Pennsylvania Press.
2. 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.
3. Llinás RR (1988) The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. Science 242: 1654-1664.
4. Connors BW, Gutnick MJ (1990) Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci 13: 99-104.
5. Hodgkin AL (1948) The local electric changes associated with repetitive action in a non-medullated axon. J Physiol. pp 165-181.
6. Ermentrout B (1996) Type I membranes, phase resetting curves, and synchrony. Neural Comput 8: 979-1001.
7. Rinzel J, Ermentrout GB (1998) Analysis of neural excitability and oscillations. In: Koch C, Segev I, eds. Methods in Neuronal Modeling: From Ions to Networks. Cambridge (Massachusetts): The MIT Press. pp 251-291.
8. Gutkin B, Ermentrout GB, Rudolph M (2003) Spike generating dynamics and the conditions for spike-time precision in cortical neurons. J Comput Neurosci 15: 91-103.
9. St Hilaire M, Longtin A (2004) Comparison of coding capabilities of type I and type II neurons. J Comput Neurosci 16: 299-313.
10. Tateno T, Harsch A, Robinson HP (2004) Threshold firing frequency-current relationships of neurons in rat somatosensory cortex: type 1 and type 2 dynamics. J Neurophysiol 92: 2283-2294.
11. Tateno T, Robinson HP (2006) Rate coding and spike-time variability in cortical neurons with two types of threshold dynamics. J Neurophysiol 95: 2650-2663.
12. Tateno T, Robinson HP (2007) Phase resetting curves and oscillatory stability in interneurons of rat somatosensory cortex. Biophys J 92: 683-695.
13. Izhikevich EM (2007) Dynamical Systems in Neuroscience. Cambridge (Massachusetts): MIT Press.
14. Prescott SA, De Koninck Y (2002) Four cell types with distinctive membrane properties and morphologies in lamina I of the spinal dorsal horn of the adult rat. J Physiol 539: 817-836.
15. Ruscheweyh R, Sandkuhler J (2002) Lamina-specific membrane and discharge properties of rat spinal dorsal horn neurones in vitro. J Physiol 541: 231-244.
16. Lopez-Garcia JA, King AE (1994) Membrane properties of physiologically classified rat dorsal horn neurons in vitro: correlation with cutaneous sensory afferent input. Eur J Neurosci 6: 998-1007.
17. Thomson AM, West DC, Headley PM (1989) Membrane characteristics and synaptic responsiveness of superficial dorsal horn neurons in a slice preparation of adult rat spinal cord. Eur J Neurosci 1: 479-488.
18. Grudt TJ, Perl ER (2002) Correlations between neuronal morphology and electrophysiological features in the rodent superficial dorsal horn. J Physiol 540: 189-207.
19. Chandler SH, Hsaio CF, Inoue T, Goldberg LJ (1994) Electrophysiological properties of guinea pig trigeminal motoneurons recorded in vitro. J Neurophysiol 71: 129-145.
20. + channels in sustained high-frequency firing of fast-spiking neocortical interneurons. J Neurophysiol 82: 2476-2489.
21. Hong S, Arcas B, Fairhall AL (2007) Single neuron computation: from dynamical system to feature detector. Neural Comput 19: 3133-3172.
22. FitzHugh R (1961) Impulses and physiological states in theoretical models of nerve membrane. Biophys J 1: 445-466.
23. FitzHugh R (1969) Mathematical models of excitation and propagation in nerve. In: Schwan HP, ed. Biological Engineering. Toronto, Canada: McGraw-Hill Book Company. pp 1-85.
24. Toledo-Rodriguez M, Blumenfeld B, Wu C, Luo J, Attali B, et al. (2004) Correlation maps allow neuronal electrical properties to be predicted from single-cell gene expression profiles in rat neocortex. Cereb Cortex 14: 1310-1327.
25. Kepler TB, Abbott LF, Marder E (1992) Reduction of conductance-based neuron models. Biol Cybern 66: 381-387.
26. Prescott SA, De Koninck Y (2005) Integration time in a subset of spinal lamina I neurons is lengthened by sodium and calcium currents acting synergistically to prolong subthreshold depolarization. J Neurosci 25: 4743-4754.
27. Borisyuk A, Rinzel J (2005) Understanding neuronal dynamics by geometrical dissection of minimal models. In: Chow C, Gutkin B, Hansel D, Meunier C, Dalibard J, eds. Methods and Models in Neurophysics, Proceedings of Les Houches Summer School Elsevier. pp 19-72.
28. Jack JJB, Noble D, Tsien RY (1975) Electric Current Flow in Excitable Cells. Oxford, UK: Clarendon Press.
29. Wilson HR (1999) Simplified dynamics of human and mammalian neocortical neurons. J Theor Biol 200: 375-388.
30. Svirskis G, Kotak V, Sanes DH, Rinzel J (2004) Sodium along with low-threshold potassium currents enhance coincidence detection of subthreshold noisy signals in MSO neurons. J Neurophysiol 91: 2465-2473.
31. Prescott SA, Ratté S, De Koninck Y, Sejnowski TJ (2008) Pyramidal neurons switch from integrators in vitro to resonators under in vivo-like conditions. J Neurophysiol. Submitted.
32. Lundstrom BN, Hong S, Higgs MH, Fairhall AL (2008) Two computational regimes of a single-compartment neuron separated by a planar boundary in conductance space. Neural Comput 20: 1239-1260.
33. Golomb D, Donner K, Shacham L, Shlosberg D, Amitai Y, Hansel D (2007) Mechanisms of firing patterns in fast-spiking cortical interneurons. PLoS Comput Biol 3: e156. doi:10.1371/journal.pcbi.0030156.
34. Agmon-Snir H, Carr CE, Rinzel J (1998) The role of dendrites in auditory coincidence detection. Nature 393: 268-272.
35. Balasubramanyan S, Stemkowski PL, Stebbing MJ, Smith PA (2006) Sciatic chronic constriction injury produces cell-type-specific changes in the electrophysiological properties of rat substantia gelatinosa neurons. J Neurophysiol 96: 579-590.
36. Miura A, Kawatani M, Araki I, de Groat WC (2000) Electrophysiological properties of lumbosacral preganglionic neurons in the neonatal rat spinal cord. Brain Res 872: 54-63.
37. Glazebrook PA, Ramirez AN, Schild JH, Shieh CC, Doan T, et al. (2002) Potassium channels Kv1.1, Kv1.2 and Kv1.6 influence excitability of rat visceral sensory neurons. J Physiol 541: 467-482.
38. Sculptoreanu A, de Groat WC (2007) Neurokinins enhance excitability in capsaicin-responsive DRG neurons. Exp Neurol 205: 92-100.
39. Wang GY, Ratto G, Bisti S, Chalupa LM (1997) Functional development of intrinsic properties in ganglion cells of the mammalian retina. J Neurophysiol 78: 2895-2903.
40. Faber ES, Callister RJ, Sah P (2001) Morphological and electrophysiological properties of principal neurons in the rat lateral amygdala in vitro. J Neurophysiol 85: 714-723.
41. Paton JF, Foster WR, Schwaber JS (1993) Characteristic firing behavior of cell types in the cardiorespiratory region of the nucleus tractus solitarii of the rat. Brain Res 604: 112-125.
42. Smith PH (1995) Structural and functional differences distinguish principal from nonprincipal cells in the guinea pig MSO slice. J Neurophysiol 73: 1653-1667.
43. + conductances with complementary functions in postsynaptic integration at a central auditory synapse. J Neurosci 15: 8011-8022.
44. Agar E, Green GG, Sanders DJ (1996) Membrane properties of mouse anteroventral cochlear nucleus neurons in vitro. J Basic Clin Physiol Pharmacol 7: 179-198.
45. Rancz EA, Ishikawa T, Duguid I, Chadderton P, Mahon S, et al. (2007) High-fidelity transmission of sensory information by single cerebellar mossy fibre boutons. Nature 450: 1245-1248.
46. + current. Proc Natl Acad Sci U S A 104: 11453-11458.
47. Rathouz M, Trussell L (1998) Characterization of outward currents in neurons of the avian nucleus magnocellularis. J Neurophysiol 80: 2824-2835.
48. Ferragamo MJ, Oertel D (2002) Octopus cells of the mammalian ventral cochlear nucleus sense the rate of depolarization. J Neurophysiol 87: 2262-2270.
49. Cao XJ, Oertel D (2005) Temperature affects voltage-sensitive conductances differentially in octopus cells of the mammalian cochlear nucleus. J Neurophysiol 94: 821-832.
50. Chéry N, Yu XH, De Koninck Y (2000) Visualization of lamina I of the dorsal horn in live adult rat spinal cord slices. J Neurosci Methods 96: 133-142.
51. Uhlenbeck GE, Ornstein LS (1930) On the theory of Brownian motion. Phys Rev 36: 823-841.
52. Morris C, Lecar H (1981) Voltage oscillations in the barnacle giant muscle fiber. Biophys J 35: 193-213.
53. Ermentrout B (2002) Simulating, Analyzing, and Animating Dynamical Systems: A Guide to Xppaut for Researchers and Students. Philadelphia: SIAM.
54. Strogatz SH (1998) Nonlinear Dynamics and Chaos: With Applications to Physics, Biology, Chemistry, and Engineering. Don Mills, Canada: Addison-Wesley.
55. Rose RM, Hindmarsh JL (1989) The assembly of ionic currents in a thalamic neuron. I. The three-dimensional model. Proc R Soc Lond B Biol Sci 237: 267-288.