Locking, intermittency, and bifurcations in a periodically driven pacemaker neuron: Poincaré maps and biological implications

Slowly adapting stretch receptor (SAO) pacemaker neurons, driven with periodic tugs, were analyzed by way of Poincaré mappings (Appendix). Two behaviors were apparent, i) Intermittency characterized previously unclear situations: discharges shifted irregularly between prolonged epochs where spike phases (relative to tugs) and intervals barely changed (slid), and brief bursts with marked variations (skipped), ii) Locking was well-known: phases and intervals remained almost fixed, regardless of the initiation. Changing frequencies, map domains with locking (ordered according to spikes/tugs ratios), alternated with intermittent ones. The best fit for any experimental map was a curve, not straight but certainly unidimensional, continuous and monotonic; it varied characteristically with frequency. This suggested relations called diffeomorphisms, implying periodicity and quasi-periodicity. Outcomes, expanding previous knowledge and meaningful biologically, were i)a precise, exhaustive behavior list (including between behavior transitions) and ii)a thorough understanding or model. This, in turn, provides norms for more specific models (single-variable ones suffice), constraints upon basic mechanisms (one variable, reflecting several real ones combined, should behave as the phase), and forecasts for future experimentation (e.g., unexamined tug frequencies and amplitudes).

[1]  J. Segundo,et al.  Stretch receptor responses to sinusoidal stimuli depend critically on modulation depth and background length , 1985, Biological Cybernetics.

[2]  G. P. Moore,et al.  PACEMAKER NEURONS: EFFECTS OF REGULARLY SPACED SYNAPTIC INPUT. , 1964, Science.

[3]  T. Teorell A Biophysical Analysis of Mechano-electrical Transduction , 1971 .

[4]  A. S. French,et al.  The frequency response, coherence, and information capacity of two neuronal models. , 1972, Biophysical journal.

[5]  J. Segundo,et al.  A model of excitatory synaptic interactions between pacemakers. Its reality, its generality, and the principles involved , 1981, Biological Cybernetics.

[6]  C A Terzuolo,et al.  Transfer functions of the slowly adapting stretch receptor organ of Crustacea. , 1965, Cold Spring Harbor symposia on quantitative biology.

[7]  M. C. Brown,et al.  Quantitative studies on the slowly adapting stretch receptor of the crayfish , 1966, Kybernetik.

[8]  W Buño,et al.  White noise analysis of pace‐maker‐response interactions and non‐linearities in slowly adapting crayfish stretch receptor. , 1984, The Journal of physiology.

[9]  Leon Glass,et al.  Bistability, period doubling bifurcations and chaos in a periodically forced oscillator , 1982 .

[10]  J. P. Segundo,et al.  Presynaptic irregularity and pacemaker inhibition , 1981, Biological Cybernetics.

[11]  B A Huberman,et al.  Chaotic behavior in dopamine neurodynamics. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[12]  R. A. Chaplain,et al.  Systems analysis of biological receptors , 1971, Kybernetik.

[13]  J. Nicholls From neuron to brain , 1976 .

[14]  A. Holden,et al.  Repetitive activity of a molluscan neurone driven by maintained currents: A supercritical bifurcation , 1981, Biological Cybernetics.

[15]  Lawrence M. Ward,et al.  On Chaotic Behavior , 1994 .

[16]  J. F. Vibert,et al.  Slowly adapting stretch-receptor organs: Periodic stimulation with and without perturbations , 1979, Biological Cybernetics.

[17]  Testing a model of excitatory interactions between oscillators , 1987, Biological Cybernetics.

[18]  E. Ott Strange attractors and chaotic motions of dynamical systems , 1981 .

[19]  J. P. Segundo,et al.  Pervasive locking, saturation, asymmetric rate sensitivity and double-valuedness in crayfish stretch receptors , 2004, Biological Cybernetics.

[20]  C. Antzelevitch,et al.  Phase resetting and annihilation of pacemaker activity in cardiac tissue. , 1979, Science.

[21]  Carme Torras I Genis Temporal-Pattern Learning in Neural Models , 1985 .

[22]  A. Holden,et al.  The response of a molluscan neurone to a cyclic input: Entrainment and phase-locking , 1981, Biological Cybernetics.

[23]  D. Petracchi,et al.  Effects of current pulses on the sustained discharge of visual cells of Limulus. , 1984, Biophysical journal.

[24]  G. P. Moore,et al.  Pacemaker Neurons: Effects of Regularly Spaced Synaptic Input , 1964, Science.

[25]  R. Wyman Multistable firing patterns among several neurons. , 1966, Journal of neurophysiology.

[26]  Y. Pomeau,et al.  Intermittent transition to turbulence in dissipative dynamical systems , 1980 .

[27]  R. Abraham,et al.  Dynamics--the geometry of behavior , 1983 .

[28]  A. Garfinkel A mathematics for physiology. , 1983, The American journal of physiology.

[29]  P. Rapp Why are so many biological systems periodic? , 1987, Progress in Neurobiology.

[30]  Pierre Bergé,et al.  Order within chaos : towards a deterministic approach to turbulence , 1984 .

[31]  J. Segundo,et al.  Respiratory oscillator entrainment by periodic vagal afferentes: An experimental test of a model , 2004, Biological Cybernetics.

[32]  L. Glass,et al.  Global bifurcations of a periodically forced biological oscillator , 1984 .

[33]  W B Matthews,et al.  From Neuron to Brain , 1976 .

[34]  W Buño,et al.  Modulation of pacemaker activity by IPSP and brief length perturbations in the crayfish stretch receptor. , 1987, Journal of neurophysiology.

[35]  J. Eckmann Roads to turbulence in dissipative dynamical systems , 1981 .

[36]  Summation of excitation and inhibition in the slowly adapting stretch receptor neuron of the crayfish , 1976, Biological Cybernetics.