Summary
-
1.
A technique was developed to measure the strength-duration relationship for action potential initiation in the rapidly adapting sensory neuron of the femoral tactile spine in the cockroach,Periplaneta americana. Extracellular current was applied via a microelectrode adjacent to the axon where it leaves the soma. A computer-controlled successive approximation algorithm reliably determined threshold levels for rectangular current pulses of varying duration.
-
2.
Experiments were conducted under resting conditions and also with constant depolarizing and hyperpolarizing base currents. Strength-duration data were well fitted by theoretical relationships derived for these conditions and assuming a constant charge threshold for the axon. The fitted equations gave values of the rheobasic current (threshold current for an infinitely long pulse) and the membrane time constant. The time constant was in good agreement with previous estimates obtained from this preparation using different techniques.
-
3.
Both the rheobasic current and the time constant were functions of the constant base current. The rheobasic current increased strongly with depolarization so that it was always more positive than the base current. This gives a quantitative explanation of the observation that no depolarizing stimulus can sustain continuous action potential firing in this neuron.
-
4.
With mild hyperpolarizing currents the rheobasic current decreased but with strong hyperpolarizations it increased and the time constant was reduced. This suggests that additional ionic conductance limits threshold behavior with strong hyperolarizations.
-
5.
Experiments with blocking agents and ionic substitution suggested that a potassium A-current is involved in the threshold behavior with strong hyperpolarizations. Some evidence for increased chloride conductance under these conditions was also obtained.
-
6.
No evidence was found that potassium or chloride currents are involved in the threshold behavior or rapid adaptation under normal or depolarized conditions.
Similar content being viewed by others
References
Adams P (1982) Voltage-dependent conductances of vertebrate neurones. TINS 5:116–119
Bohnenberger J (1981) Matched transfer characteristics of single units in a compound slit sense organ. J Comp Physiol 142:391–402
Boyd IA, Gladden MJ, Ward J (1977) The contribution of intrafusal creep to the dynamic component of the Ia afferent discharge of isolated muscle spindles. J Physiol 273:27–28P
Brown MC, Stein RB (1966) Quantitative studies on the slowly adapting stretch receptor of the crayfish. Kybernetik 3:175–185
Catton WT, Petoe N (1966) A visco-elastic theory of mechanoreceptor adaptation. J Physiol 187:35–49
Chapman KM, Smith RS (1963) A linear transfer function underlying impulse frequency modulation in a cockroach mechanoreceptor. Nature 197:699–700
Chesler M, Fourtner CR (1981) Mechanical properties of a slow muscle in the cockroach. J Neurobiol 12:391–402
Chesnoy-Marchais D (1982) A chloride conductance activated by hyperpolarization inAplysia neurones. Nature 299:359–361
Eyzaguirre C, Kuffler SW (1955) Processes of excitation in the dendrites and in the soma of single isolated sensory nerve cells of the lobster and crayfish. J Gen Physiol 39:87–119
French AS (1984a) Action potential adaptation in the femoral tactile spine of the cockroach,Periplaneta americana. J Comp Physiol A 155:803–812
French AS (1984b) The receptor potential and adaptation in the cockroach tactile spine. J Neurosci 4:2063–2068
French AS (1985a) The effects of temperature on action potential encoding in the cockroach tactile spine. J Comp Physiol A 156:817–821
French AS (1985) After-hyperpolarization and receptor potential attenuation following bursts of action potentials in an insect mechanoreceptor. Can J Physiol Pharmacol 63:18–22
French AS (1986) The role of calcium in the rapid adaptation of an insect mechanoreceptor. J Neurosci 6:2322–2326
French AS, Sanders EJ (1981) The mechanosensory apparatus of the femoral tactile spine of the cockroach,Periplaneta americana. Cell Tissue Res 219:53–68
Gestrelius S, Grampp W, Sjolin L (1981) Subthreshold and near-threshold membrane currents in lobster stretch receptor neurones. J Physiol 310:191–203
Gilly WF, Armstrong CM (1984) Threshold channels — a novel type of sodium channel in squid giant axon. Nature 309:448–450
Hille B (9184) Ionic channels of excitable membranes. Sinauer Associates, Sunderland, Massachusetts
Hunt CC, Wilkinson RS (1980) An analysis of receptor potential and tension of isolated cat muscle spindles in response to sinusoidal stretch. J Physiol 302:241–262
Jack JJB, Noble D, Tsien RW (1983) Electric current flow in excitable cells. Oxford University Press, Oxford
Landgren S (1953) On the excitation mechanism of the carotid baroreceptors. Acta Physiol Scand 26:1–34
Lapique L (1907) Recherches quantitatifs sur l'excitation électrique des nerfs traitée comme une polarisation. J Physiol Paris 9:622–635
Lewis DV, Wilson WA (1982) Calcium influx and poststimulus current during early adaptation inAplysia giant neurons. J Neurophysiol 48:202–216
Loewenstein WR (1956) Excitation and changes in adaptation by stretch of mechanoreceptors. J Physiol 133:588–602
Matteson DR, Armstrong CM (1982) Evidence for a population of sleepy sodium channels in squid axon at low temperature. J Gen Physiol 79:739–758
Mendelson M, Loewenstein WR (1964) Mechanisms of receptor adaptation. Science 144:554–555
Mountcastle VB, LaMotte RH, Carli G (1972) Detection threshold for stimuli in humans and monkeys: comparison with threshold events in mechanoreceptive afferent nerve fibres innervating monkey hand. J Neurophysiol 35:122–136
Nakajima S, Onodera K (1969) Membrane properties of the stretch receptor neurones of crayfish with particular reference to mechanisms of sensory adaptation. J Physiol 200:161–185
Noble D, Stein RB (1966) The threshold conditions for initiation of action potentials by excitable cells. J Physiol 187:129–162
Ottoson D, Swerup C (1985a) Ionic dependence of early adaptation in the crustacean stretch receptor. Brain Res 336:1–8
Ottoson D, Swerup C (1985b) Effects of intracellular TEA injection on early adaptation of crustacean stretch receptor. Brain Res 336:9–17
Pubols BH, Pubols LM (1983) Tactile receptor discharge and mechanical properties of glabrous skin. Fed Proc 42:2528–2535
Rang HP, Ritchie JM (1968) On the electrogenic sodium pump in mammalian non-myelinated nerve fibres and its activation by various external cations. J Physiol 196:183–221
Rogawski MA (1985) The A-current: how ubiquitous a feature of excitable cells is it? TINS 8:214–219
Vallbo AB (1963) Accommodation related to inactivation of the sodium permeability in single myelinated nerve fibres fromXenopus laevis. Acta Physiol Scand 61:429–444
Yawo H, Kojima H, Kuno M (1985) Low-threshold slow-inactivating sodium potentials in the cockroach giant axon. J Neurophysiol 54:1087–1100
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
French, A.S. Strength-duration properties of a rapidly adapting insect sensory neuron. J. Comp. Physiol. 159, 757–764 (1986). https://doi.org/10.1007/BF00603729
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00603729