Random-sequence stimulation of the G1 hair afferent unit.

Impulse trains were recorded from the parent axon of the cat G1 hair afferent unit. Separate random (Poisson-like) trains of mechanical stimuli were applied to two coinnervated receptive field hairs individually or concurrently. The objective was to determine whether the parent axonal impulse train elicited by dual-hair stimulation was due to a temporal combining ("mixing"; Fukami, 1980) of the impulse trains elicited in the parent axons by the same stimulation to each hair alone. Both impulse rates and patterns were assessed. During single-hair random stimulation, impulse trains differed from stimulus trains, having lower mean rates and short-interval doublets. During dual-hair random stimulation, mean impulse frequencies were on average 36% less than those predicted for mixing. There were no correlations between stimulus amplitude and departures from mixing. As a further test of the mixing hypothesis, the two single-hair-elicited impulse trains were temporally merged (i.e., superimposed to form one impulse train). Such merged impulse trains were compared with the corresponding dual-hair-elicited impulse train. Dual-hair-elicited frequencies were typically less than those of the merged trains, despite the use of an absolute-refractory-period criterion during merging. The impulse patterns elicited by dual-hair stimulation usually differed from the merged-train patterns. Temporal coupling between stimuli and impulses was either variable or absent during single-hair random stimulation; such coupling was altered during dual-hair random stimulation. In summary, this work showed that the dual-hair responses could not be predicted from the single-hair responses. Limitations of the mixing hypothesis and possible biophysical mechanisms in the axonal arborization are discussed. The results are consistent with a general hypothesis of analog processing within the arborization of the parent axon.

[1]  S. S. Tower UNIT FOR SENSORY RECEPTION IN CORNEA , 1940 .

[2]  Fatigue in cat facial mechanoreceptors , 1982, Neuroscience Letters.

[3]  Response of forelimb guard hair afferent units to air-jet stimulation of entire receptive field. , 1980, Journal of neurophysiology.

[4]  M. Westerfield,et al.  Temperature-sensitive conduction failure at axon branch points. , 1978, Journal of neurophysiology.

[5]  Lindlom Uf Excitability and functional organization within a peripheral tactile unit. , 1958, Acta physiologica Scandinavica. Supplementum.

[6]  S. Miller Excitation of mechanoreceptor units in the skin of the rabbit ear. , 1967, Archives italiennes de biologie.

[7]  Gerald E. Loeb,et al.  Optimal control principles for sensory transducers , 1985 .

[8]  M. D. Goldfinger,et al.  Contributions by individual guard hairs and their interactions in response of forelimb guard hair afferent unit. , 1980, Journal of neurophysiology.

[9]  P R Burgess,et al.  Receptor types in cat hairy skin supplied by myelinated fibers. , 1968, Journal of neurophysiology.

[10]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. , 1967, Biophysical journal.

[11]  M. Aoki Distal slowing of conduction in forelimb and hindlimb myelinated cutaneous afferent fibers in cat , 1977, Experimental Neurology.

[12]  M. D. Goldfinger Poisson process stimulation of an excitable membrane cable model. , 1986, Biophysical journal.

[13]  A W Goodwin,et al.  Single quickly adapting mechanoreceptive afferents innervating monkey glabrous skin: response to two vibrating probes. , 1981, Journal of neurophysiology.

[14]  R. Purple,et al.  Afferent fibers with multiple encoding sites. , 1974, Brain research.

[15]  K W Horch,et al.  Impulse generation in type I cutaneous mechanoreceptors. , 1974, Journal of neurophysiology.

[16]  J. Lettvin,et al.  Multiple meaning in single visual units. , 1970, Brain, behavior and evolution.

[17]  R. W. Banks,et al.  Form and distribution of sensory terminals in cat hindlimb muscle spindles. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[18]  F.J. Looft,et al.  Interdome interactions in cutaneous Type I receptors , 1988, IEEE Transactions on Biomedical Engineering.

[19]  Interaction of activity in frog skin touch afferent units. , 1981, Journal of neurophysiology.

[20]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. I. The single spike train. , 1967, Biophysical journal.

[21]  R. H. Ray,et al.  The response of single guard and down hair mechanoreceptors to moving air-jet stimulation , 1985, Brain Research.

[22]  I. Parnas,et al.  Differential conduction block in branches of a bifurcating axon. , 1979, The Journal of physiology.

[23]  B H Matthews,et al.  The response of a muscle spindle during active contraction of a muscle , 1931, The Journal of physiology.

[24]  F. Ito,et al.  Structural and functional asymmetries of myelinated branches in the frog muscle spindle , 1974, The Journal of physiology.

[25]  G. P. Moore,et al.  Statistical analysis and functional interpretation of neuronal spike data. , 1966, Annual review of physiology.

[26]  S. S. Tower Action potentials in sympathetic nerves, elicited by stimulation of frog's viscera , 1933, The Journal of physiology.

[27]  S. Stoney,et al.  Unequal branch point filtering action in different types of dorsal root ganglion neurons of frogs , 1985, Neuroscience Letters.

[28]  B. Munger Patterns of Organization of Peripheral Sensory Receptors , 1971 .

[29]  W. T. Catton,et al.  Threshold, recovery and fatigue of tactile receptors in frog skin , 1961, The Journal of physiology.

[30]  P. R. Burgess,et al.  Cutaneous Mechanoreceptors and Nociceptors , 1973 .

[31]  William H. Calvin,et al.  Impulses reflected from dorsal root ganglia and from focal nerve injuries , 1976, Brain Research.

[32]  E. Barrett,et al.  Intracellular recording from vertebrate myelinated axons: mechanism of the depolarizing afterpotential , 1982, The Journal of physiology.

[33]  D. Tapper,et al.  Integration of impulse activity in a peripheral sensory unit. , 1966, Experimental neurology.

[34]  A. Blight,et al.  Computer simulation of action potentials and afterpotentials in mammalian myelinated axons: The case for a lower resistance myelin sheath , 1985, Neuroscience.

[35]  A. Paintal,et al.  Effects of temperature on conduction in single vagal and saphenous myelinated nerve fibres of the cat. , 1965, The Journal of physiology.

[36]  R. Llinás The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. , 1988, Science.

[37]  B. Munger,et al.  The terminal myelin segments of afferent axons to cutaneous mechanoreceptors , 1985, Brain Research.

[38]  C. Stevens,et al.  Prediction of repetitive firing behaviour from voltage clamp data on an isolated neurone soma , 1971, The Journal of physiology.

[39]  R. Tuckett Response of cutaneous hair and field mechanoreceptors in cat to paired mechanical stimuli. , 1978, Journal of neurophysiology.

[40]  B. Lynn,et al.  Effects of sympathetic stimulation on mechanoreceptive and nociceptive afferent units from the rabbit pinna , 1986, Brain Research.

[41]  永野 俊雄,et al.  The Mechanoreceptors of the Mammalian Skin., Ultrastructure and Morphological Calssification., Z. Halata , Adv. in Anat. Embryol. Cell Biol. 50(5), 1-77, 1975., Springer-Verlag, Berlin, Heidelberg, New York(らいぶらりい) , 1975 .

[42]  E. Adrian,et al.  Sensory discharges in single cutaneous nerve fibres , 1931, The Journal of physiology.

[43]  U Proske,et al.  Site of impulse initiation in tendon organs of cat soleus muscle. , 1985, Journal of neurophysiology.

[44]  H. Swadlow,et al.  Modulation of impulse conduction along the axonal tree. , 1980, Annual review of biophysics and bioengineering.

[45]  W Rall,et al.  Changes of action potential shape and velocity for changing core conductor geometry. , 1974, Biophysical journal.

[46]  I. Tasaki Collision of two nerve impulses in the nerve fibre , 1949 .

[47]  P. R. Burgess,et al.  Dorsal column projection of receptors in cat hairy skin supplied by myelinated fibers. , 1968, Journal of neurophysiology.

[48]  K W Horch,et al.  A key to the classification of cutaneous mechanoreceptors. , 1977, The Journal of investigative dermatology.

[49]  F. T. Dun The delay and blockage of sensory impulses in the dorsal root ganglion * , 1955, The Journal of physiology.

[50]  Y. Fukami Interaction of impulse activities originating from individual Golgi tendon organs innervated by branches of a single axon. , 1980, The Journal of physiology.

[51]  A. R. Muir,et al.  The structure and function of a slowly adapting touch corpuscle in hairy skin , 1969, The Journal of physiology.

[52]  G. Poggio,et al.  TIME SERIES ANALYSIS OF IMPULSE SEQUENCES OF THALAMIC SOMATIC SENSORY NEURONS. , 1964, Journal of neurophysiology.

[53]  H. D. Miller,et al.  The Theory Of Stochastic Processes , 1977, The Mathematical Gazette.

[54]  J. Hindmarsh,et al.  A model of a thalamic neuron , 1985, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[55]  A note on the use of serial measures in spike train analysis and their relation to the corresponding moments. , 1983, The International journal of neuroscience.

[56]  K. Horch,et al.  Response of cutaneous hair and field mechanoreceptors in cat to threshold stimuli. , 1978, Journal of neurophysiology.

[57]  N. Stockbridge Differential conduction at axonal bifurcations. II. Theoretical basis. , 1988, Journal of neurophysiology.

[58]  B. Katz Action potentials from a sensory nerve ending , 1950, The Journal of physiology.

[59]  P. Grigg Biophysical studies of mechanoreceptors. , 1986, Journal of applied physiology.

[60]  Axonal branch shapes , 1985, Brain Research.