Summary
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1.
Adaptation of action potential discharge was studied in the sensory neuron of a rapidly adapting insect mechanoreceptor, the cockroach,Periplaneta americana, femoral tactile spine. Direct electrical stimulation of the neuron was achieved by passing current through a micro-electrode adjacent to the axon where it leaves the soma. Action potentials were monitored extracellularly further along the axon.
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2.
The dynamic properties of action potential generation were observed in response to steps of current and to randomly varying currents. The step and frequency responses could both be well fitted by power-laws, which were indistinguishable from the behavior observed during mechanical stimulation of the spine.
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3.
Electrical stimulation of the axon further from the soma also gave a power-law response, suggesting that this dynamic behavior reflects general properties of the axon membrane, rather than a specific initiation site.
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4.
Variations in stimulus amplitude caused large changes in the rates of adaptation to steps or random stimuli. However, these changes were in opposite directions for the two types of stimulus.
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5.
Depolarization by addition of a DC current to the stimuli caused increases in the rates of adaptation to steps and random stimuli. Hyperpolarization caused the opposite effects. Raising the external potassium concentration also increased the rates of adaptation while decreasing potassium concentration caused the opposite effects.
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6.
The results indicate that adaptation in this receptor occurs during action potential initiation. Although the adaptation is well characterized by a power-law, the parameters vary with the type of stimulus, stimulus strength, and mean polarization level. These strong nonlinearities are difficult to explain by the distributed parameter linear models which are usually invoked to account for power-law behaviour.
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Abbreviations
- rms :
-
root mean square
- imp :
-
impulses
References
Bernard J, Guillet JC, Coillot JP (1980) Evidence for a barrier between blood and sensory terminal in an insect mechano-receptor. Comp Biochem Physiol 67A:573–579
Biederman-Thorson M, Thorson J (1971) Dynamics of excitation and inhibition in the light adaptedLimulus eye. J Gen Physiol 58:1–19
Bohnenberger J (1981) Matched transfer characteristics of single units in a compound slit sense organ. J Comp Physiol 142:391–402
Brown MC, Stein RB (1966) Quantitative studies on the slowly adapting stretch receptor of the crayfish. Kybernetik 3:175–185
Chapman KM, Smith RS (1963) A linear transfer function underlying impulse frequency modulation in a cockroach mechanoreceptor. Nature 197:699–700
Chapman KM, Mosinger JL, Duckrow RB (1979) The role of viscoelastic coupling in sensory adaptation in an insect mechanoreceptor. J Comp Physiol 131:1–12
Chesler M, Fourtner CR (1981) Mechanical properties of a slow muscle in the cockroach. J Neurobiol 12:391–402
Erler G, Thurm U (1981) Dendritic impulse initiation in an epithelial sensory neuron. J Comp Physiol 142:237–249
Fohlmeister JF (1973) A model for phasic and tonic repetitively firing neural encoders. Kybernetik 13:104–112
Fohlmeister JF, Poppele RE, Purple RL (1977) Repetitive firing: A quantitative study of feedback in model encoders. J Gen Physiol 69:815–858
French AS (1973) Automated spectral analysis of neurophysiological data using intermediate magnetic tape storage. Cornput Prog Biomed 3:45–57
French AS (1980) Sensory transduction in an insect mechanoreceptor: linear and nonlinear properties. Biol Cybern 38:115–123
French AS (1984a) The dynamic properties of the action potential encoder in an insect mechanosensory neuron. Biophys J 146:285–290
French AS (1984b) The receptor potential and adaptation in the cockroach tactile spine. J Neurosci 4:2063–2068
French AS, Holden AV (1971) Alias-free sampling of neuronal spike trains. Kybernetik 8:165–171
French AS, Kuster JE (1981) Sensory transduction in an insect mechanoreceptor: extended bandwidth measurements and sensitivity to stimulus strength. Biol Cybern 42:87–94
French AS, Sanders EJ (1981) The mechanosensory apparatus of the femoral tactile spine of the cockroach,Periplaneta americana. Cell Tissue Res 219:53–68
French AS, Holden AV, Stein RB (1972) The estimation of the frequency response function of a mechanoreceptor. Kybernetik 11:15–23
Gestrelius S, Grampp W (1983) Impulse firing in the slowly adapting stretch receptor neurone of lobster and its numerical simulation. Acta Physiol Scand 118:253–261
Guillet JC, Bernard J, Coillot JP, Callec JJ (1980) Electrical properties of the dendrite in an insect mechanoreceptor: effects of antidromic or direct electrical stimulation. J Insect Physiol 26:755–762
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
Kuster JE, French AS (1983) Sensory transduction in a locust multipolar joint receptor: the dynamic behavior under a variety of stimulus conditions. J Comp Physiol 150:207–215
Landgren S (1953) On the excitation mechanism of the carotid baroreceptors. Acta Physiol Scand 26:1–34
Landolt JP, Correia MJ (1980) Neurodynamic response analysis of anterior semicircular canal afferents in the pigeon. J Neurophysiol 43:1746–1770
Lewis DV, Wilson WA (1982) Calcium influx and poststimulus current during early adaptation inAplysia giant neurons. J Neurophysiol 48:202–216
Marmarelis PZ, Marmarelis VZ (1978) Analysis of physiological systems, the white noise approach. Plenum Press, New York
McIver SB (1975) Structure of cuticular mechanoreceptors of arthropods. Annu Rev Entomol 20:381–397
Mendelson M, Loewenstein WR (1964) Mechanisms of receptor adaptation. Science 144:554–555
Michaelis B, Chaplain RA (1973) The encoder mechanism of receptor neurons. Kybernetik 13:6–23
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 references to mechanisms of sensory adaptation. J Physiol 200:161–185
Oldham KB, Spanier J (1974) The fractional calculus. Academic Press, New York
Ottoson D, Swerup C (1982) Studies on the role of calcium in adaptation of the crustacean stretch receptor. Effects of intracellular injection of calcium, EGTA and TEA. Brain Res 244:337–341
Poppele RE, Chen WJ (1972) Repetitive firing behavior of mammalian muscle spindle. J Neurophysiol 35:357–364
Pringle JWS, Wilson VJ (1952) The response of a sense organ to a harmonic stimulus. J Exp Biol 29:220–234
Rice MJ (1975) Insect mechanoreceptor mechanisms. In: Galun R, Hillman P, Parnas I, Werman R (eds) Sensory physiology and behavior. Plenum Press, New York, pp 135–165
Seyfarth E, Bohnenberger J, Thorson J (1982) Electrical and mechanical stimulation of a spider slit sensillum: outward current excites. J Comp Physiol 147:423–432
Sokolove PG, Cooke IM (1971) Inhibition of impulse activity in a sensory neuron by an electrogenic pump. J Gen Physiol 57:125–163
Spekreijse H, Oosting H (1970) Linearizing: a method for analysing and synthesizing non-linear systems. Kybernetik 7:22–31
Thorson J (1966) Small-signal analysis of a visual reflex in the locust. II. Frequency dependence. Kybernetik 3:53–66
Thorson J, Biedermann-Thorson M (1974) Distributed relaxation phenomena in sensory adaptation. Science 183:161–172
Tomko DL, Peterka RJ, Schor RH, O'Leary DP (1981) Response dynamics of horizontal canal afferents in barbiturate-anesthetized cats. J Neurophysiol 45:376–396
Vallbo AB (1964) Accommodation related to inactivation of the sodium permeability in single myelinated nerve fibres fromXenopus laevis. Acta Physiol Scand 61:429–444
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French, A.S. Action potential adaptation in the femoral tactile spine of the cockroach,Periplaneta americana . J. Comp. Physiol. 155, 803–812 (1984). https://doi.org/10.1007/BF00611597
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DOI: https://doi.org/10.1007/BF00611597