Skip to main content
Log in

Theoretical studies of impulse propagation in serotonergic axons

  • Published:
Biological Cybernetics Aims and scope Submit manuscript

Abstract

Impulse propagation in small-diameter (1–3 μm) axons with inhomogeneous geometry was simulated. The fibres were represented by a series of 3 μm-long compartments. The cable equation was solved for each compartment by a finite-difference approximation (Cooley and Dodge 1966). First-order differential equations governing temporal changes in membrane potential or Hodgkin-Huxley (1952) conductance parameters were solved by numerical integration. It was assumed that varicosity and intervaricosity segments had the same specific cable constants and excitability properties, and differed only in length and diameter. A single long varicosity or a ‘clump’ of 3 μm-long varicosities changed the point-to-point (axial) conduction velocity within as well as to either side of the geometrically inhomogeneous regions. When 2 μm-diameter, 3 μm-long varicosities were distributed over the 1 μm-diameter fiber length as observed in serotonergic axons, mean axial conduction velocity was between that of uniform-diameter 1 and 2 μm fibers, and changed predictably with different cable parameters. Fibers with inexcitable varicosity membranes also supported impulse propagation. These simulations provided a general theoretical basis for the slow (< 1 M/s) conduction velocity attributed to small-diameter unmyelinated varicose axons.

This is a preview of subscription content, log in via an institution to check access.

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adelman WJ, FitzHugh R (1975) Solutions of the HH equations modified for potassium accumulation in the periaxonal space. Fed Am Soc Exp Biol Proc 34:1322–1329

    Google Scholar 

  • Baker M, Bostock H, Grafe P, Martius P (1987) Function and distribution of three types of rectifying channel in rat spinal root myelinated axons. J Physiol (London) 383:45–67

    Google Scholar 

  • Basbaum AI, Zahs K, Lord B, Lakos S (1988) The fiber caliber of 5-HT immunoreactive axons in the dorsolateral funiculus of the spinal cord of the rat and cat. Somatosens Res 5:177–185

    Google Scholar 

  • Beaudet A, Descarries L (1987) Ultrastructural identification of serotonin neurons. In: Steinbusch HWM (eds) Monoaminergic neurons: light microscopy and ultrastructure, chap 9. Wiley, New York pp 265–313

    Google Scholar 

  • Black JA, Kocsis JD, Waxman SG (1990) Ion channel organization of the myelinated fiber. TINS 13:48–54

    Google Scholar 

  • Brown D (1988) M currents: an update. TINS 11:294–299

    Google Scholar 

  • Chang DC (1986) Is the K permeability of the resting membrane controlled by the excitable K channel. Biophys J 50:1095–1100

    Google Scholar 

  • Chiodo LA (1988) Dopamine-containing neurons in the mammalian central nervous system: electrophysiology and pharmacology. Neurosci Biobehav Rev 12:49–91

    Google Scholar 

  • Chiu SY, Ritchie JM, Rogart RB, Stagg D (1979) A quantitative description of membrane currents in rabbit myelinated nerve. J Physiol (London) 292:149–166

    Google Scholar 

  • Connor AJ, Stevens CF (1971) Voltage clamp studies of a transient outward membrane current in gastropod neural somata. J Physiol (London) 213:21–30

    Google Scholar 

  • Cooley JW, Dodge FA Jr (1966) Digital computer solutions for excitation and propagation of the nerve impulse. Biophys J 6:683–599

    Google Scholar 

  • Cronin J (1987) Mathematical aspects of Hodgkin-Huxley neural theory. Cambridge University Press Cambridge

    Google Scholar 

  • Deitzel ID, Drapeau P, Nicholls JG (1986) Voltage dependence of 5-hydroxytryptamine release at a synapse between identified leech neurones in culture. J Physiol (London) 372:191–205

    Google Scholar 

  • Ellias SA, Greenberg M, Stevens JK (1985) Active and passive propagation in inhomogenous axons: Theoretical and serial EM studies of varicose unmyelinated nerves. Soc Neurosci (abstr) 11:625

    Google Scholar 

  • Eng DL, Gordon TR, Kocsis JD, Waxman SG (1990) Current-clamp analysis of a time-dependent rectification in rat optic nerve. J Physiol 421:185–202

    Google Scholar 

  • Faber DS, Korn H (1986) Instantaneous inward rectification in the Mauthner cell: a postsynaptic booster for excitatory inputs. Neuroscience 19:1037–1043

    Google Scholar 

  • FitzHugh R (1962) Computation of impulse initiation and saltatory conduction in a myelinated nerve fiber. Biophys J 2:11–21

    Google Scholar 

  • Fleshman JW, Segev I, Burke RE (1988) Electronic architecture of type-identified alpha-motoneurons in the cat spinal cord. J Neurophysiol 60:60–85

    Google Scholar 

  • Forsythe ID, Redman SJ (1988) The dependence of motoneurone membrane potential on extracellular ion concentrations studied in isolated rat spinal cord. J Physiol (London) 404:83–99

    Google Scholar 

  • Gasser HS (1950) Unmedullated fibers originating in dorsal root ganglia. J Gen Physiol 33:651–690

    Google Scholar 

  • Gilly WF, Armstrong CM (1984) Threshold channels — a novel type of sodium channel in squid giant axon. Nature 309:448–450

    Google Scholar 

  • Goldfinger MD (1978) Propagated responses in nerve and muscle cable models. Brain Theory Newslett 3:63–65

    Google Scholar 

  • Goldfinger MD (1986) Poisson process stimulation of an excitable membrane cable model. Biophys J 50:27–40

    Google Scholar 

  • Goldfinger MD, Simpson CW, Resch GE (1984) Recovery by pushpull perfusion of neurochemicals released within the cuneate nucleus of the cat by somatosensory stimulation. Pharm Biochem Behav 21:117–123

    Google Scholar 

  • Goldfinger MD, Roettger VR, Pearson JC (1988) Theory of impulse propagation in cat cuneate nucleus axons with serotonin-like immunoreactivity. Soc Neurosci (abstr) 14:125

    Google Scholar 

  • Goldman L, Albus JS (1968) Computation of impulse conduction in myelinated nerve fibers; theoretical basis of velocity-diameter relation. Biophys J 8:596–607

    Google Scholar 

  • Goldstein SS, Rall W (1974) Changes in action potential shape and velocity for changing core conductor geometry. Biophys J 14:731–757

    Google Scholar 

  • Gordon TR, Kocsis JD, Waxman SG (1988) Evidence for the presence of two types of potassium channels in the rat optic nerve. Brain Res 447:1–9

    Google Scholar 

  • Hammond DL, Tyce GM, Yaksh TL (1985) Efflux of 5-hydroxytryptamine and noradrenaline into spinal cord superfusates during stimulation of the rat medulla. J Physiol (London) 359:151–162

    Google Scholar 

  • Haydon DA, Requena J, Simon AJB (1988) The potassium conductance of the resting squid axon and its blockage by clinical concentrations of general anesthetics. J Physiol (London) 402:363–374

    Google Scholar 

  • Hines M (1984) Efficient computation of branched nerve equations. Int J Bio-Med Comput 15:69–76

    Google Scholar 

  • Hodgkin AL (1954) A note on conduction velocity. J Physiol (London) 125:221–224

    Google Scholar 

  • Hodgkin AL (1975) The optimum density of sodium channels in an unmyelinated nerve. Proc Trans R Soc Lond B 270:297–300

    Google Scholar 

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

    Google Scholar 

  • Hodgkin AL, Rushton WAH (1946) The electrical constants of a crustacean nerve fibre. Proc R Soc (Ser B) 133:444–479

    Google Scholar 

  • Hornung J-P, Fritschy J-M, Tork I (1990) Distribution of two morphologically distinct subsets of serotonergic axons in the erebral cortex of the marmoset. J Comp Neurol 297:165–181

    Google Scholar 

  • Khodorov BI, Timin EN (1975) Nerve impulse along non-uniform fibers (Investigations using mathematical models). Prog Biophys Mol Biol 30:145–184

    Google Scholar 

  • King JS, Ho RH, Burry RW (1984) The distribution and synaptic organization of serotonergic elements in the inferior olivary complex of the opossum. J Comp Neurol 227:357–368

    Google Scholar 

  • Koerber HR, Druzinsky RE, Mendell LM (1988) Properties of somata of spinal dorsal root ganglion cells differ according to peripheral receptor innervated. J Neurophysiol 60:1584–1596

    Google Scholar 

  • Kosofsky BE, Molliver ME (1987) The serotonergic innervation of the cerebral cortex: Different classes of axon terminals arise from dorsal and median raphe nuclei. Synapse 1:153–168

    Google Scholar 

  • Llano I, Webb CK, Bezanilla F (1988) Potassium conductance of the squid giant axon. Single channel studies. J Gen Physiol 92:179–196

    Google Scholar 

  • Llinás RR (1988) The intrinsic electrophysiological properties of mammalian neurons: Insights into central nervous system function. Science 242:1654–1664

    Google Scholar 

  • Mascagni MV (1989) Numerical methods for neuronal modeling. In: Koch C, Segev I (eds) Methods in neuronal modeling, chap 13. MIT Press, Cambridge

    Google Scholar 

  • Miletic V, Hoffert MJ, Ruda MA, Dubner R, Shigenaga Y (1984) Serotonergic axonal contacts on identified cat spinal dorsal horn neurons and their correlation with Nucleus Raphe Magnus stimulation. J Comp Neurol 228:129–141

    Google Scholar 

  • Moore JW (1987) Computer simulations as a component of a neuroscience research program. In: Computational Neuroscience (Short Course Syllabus; Arbib MA, George SA, organizers). Society for Neuroscience, Washington, DC

    Google Scholar 

  • Moore JW, Ramon F, Joyner RW (1975) Axon voltage-clamp simulations I. Methods and tests. Biophys J 15:11–24

    Google Scholar 

  • Mulligan KA, Tork I (1987) Serotonergic axons form basket-like terminals in cerebral cortex. Neurosci Lett 81:7–12

    Google Scholar 

  • Mulligan KA, Tork I (1988) Serotonergic innervation of the cat cerebral cortex. J Comp Neurol 270:86–110

    Google Scholar 

  • Nishikawa N, Bennett GJ, Ruda MA, Lu G-W, Dubner R (1983) Immunocytochemical evidence for a serotonergic innervation of dorsal column post-synaptic neurons in cat and monkey: light- and electron-microscopic observations. Neuroscience 10:1333–1340

    Google Scholar 

  • Paintal AS (1967) A comparison of the nerve impulses of mammalian non-medullated nerve fibers with those of the smallest diameter medullated fibers. J Physiol (London) 193:523–533

    Google Scholar 

  • Papadopoulos GC, Parnavelas JG, Buijs RM (1987) Light and electron microscopic immunocytochemical analysis of the serotonin innervation of the rat visual cortex. J Neurocytol 16:883–892

    Google Scholar 

  • Pearson JC, Goldfinger MD (1987) The morphology and distribution of serotonin-like immunoreactive fibers in the cat dorsal column nuclei. Neurosci Lett 74:125–131

    Google Scholar 

  • Press WH, Flannery BP, Teukolsky SA, Vetterling WT (1986) Numerical recipes: the art of scientific computing. Cambridge University Press, Cambridge

    Google Scholar 

  • Preston RJ, Waxman SG, Kocsis JD (1983) Effects of 4-Aminopyridine on rapidly and slowly conducting axons of rat corpus callosum. Exp Neurol 79:808–820

    Google Scholar 

  • Pumphrey RJ, Young JZ (1938) The rates of conduction of nerve fibers of various diameters in cephalopods. J Exp Biol 15:453–467

    Google Scholar 

  • Qian N, Sejnowski TJ (1989) An electro-diffusion model for computing membrane potentials and ionic concentrations in branching dendrites, spines, and axons. Biol Cybern 62:1–15

    Google Scholar 

  • Rall W (1977) Core conductor theory and cable properties of neurons. In: Brookhart JM, Mountcastle VB (eds) Cellular biology of neurons, vol I: Handbook of physiology — the nervous system. I. American Physiological Society Bethesda MD, pp 39–97

    Google Scholar 

  • Ramón F, Joyner RW, Moore JW (1975) Propagation of action potentials in inhomogeneous axon regions. Fed Proc 34:1357–1363

    Google Scholar 

  • Ramón F, Moore JW, Joyner RW, Westerfield M (1976) Squid giant axons — a model for the neuron soma? Biophys J 16:953–963

    Google Scholar 

  • Segev I (1990) Computer study of presynaptic inhibition controlling the spread of action potentials into axonal terminals. J Neurophysiol 63:987–998

    Google Scholar 

  • Sorkin LS, Steinman JL, Hughes MG, Willis WD, McAdoo DJ (1988) Microdyalysis recovery of serotonin released in the spinal dorsal horn. J Neurosci Methods 23:131–138

    Google Scholar 

  • Soubrié P, Resine TD, Glowinski J (1984) Functional aspects of serotonin transmission in the basal ganglia: a review and an in-vivo approach using the push-pull cannula technique. Neuroscience 13:605–625

    Google Scholar 

  • Sprouse JS, Aghajanian GK (1987) Electrophysiological responses of serotonergic dorsal raphe neurons to 5-HT1A and 5-HT1B Agonists. Synapse 1:3–9

    Google Scholar 

  • Steinbusch HWM (1981) Distribution of serotonin-immunoreactivity in the central nervous system of the rat-cell bodies and terminals. Neuroscience 6:557–618

    Google Scholar 

  • Tyce GM, Yaksh TL (1981) Monoamine release from cat spinal cord by somatic stimuli: an intrinsic modulatory system. J Physiol (London) 314:513–529

    Google Scholar 

  • Walmsley B, Nicol MJ (1990) Synaptic transmission in the mammalian central nervous system. In: Rowe M, Aitkin C (eds) Information processing in mammalian auditory and tactile systems. Neurology & Neurobiology, vol 56. Wiley-Liss, New York, pp 97–110

    Google Scholar 

  • Wessendorf MW, Anderson EG (1983) Single unit studies of identified bulbospinal serotonergic units. Brain Res 279:93–103

    Google Scholar 

  • Wessendorf MW, Proudfit HK, Anderson EG (1981) The identification of serotonergic neurons in the nucleus raphé magnus by conduction velocity. Brain Res 214:168–173

    Google Scholar 

  • Williams JT, Colmers WF, Pan ZZ (1988) Voltage- and ligand-activated inwardly rectifying currents in dorsal Raphe neurons in vitro. J Neurosci 8:3499–3506

    Google Scholar 

  • Yamada WM, Koch C, Adams PR (1989) Multiple channels and calcium dynamics. In: Koch C, Segev I (eds) Methods in neuronal modeling, chap 4. MIT Press, Cambridge

    Google Scholar 

  • Zill DG (1986) A first course in differential equations with applications. Third edn. PWS, Boston

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Goldfinger, M.D., Roettger, V.R. & Pearson, J.C. Theoretical studies of impulse propagation in serotonergic axons. Biol. Cybern. 66, 399–406 (1992). https://doi.org/10.1007/BF00197719

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00197719

Keywords

Navigation