Nonlinear neuronal mode analysis of action potential encoding in the cockroach tactile spine neuron

Neuronal mode analysis is a recently developed technique for modelling the behavior of nonlinear systems whose outputs consist of action potentials. The system is modelled as a set of parallel linear filters, or modes, which feed into a multi-input threshold. The characteristics of the principal modes and the multi-input threshold device can be derived from Laguerre function expansions of the computed first- and second-order Volterra kernels when the system is stimulated with a randomly varying input. Neuronal mode analysis was used to model the encoder properties of the cockroach tactile spine neuron, a nonlinear, rapidly adapting, sensory neuron with reliable behavior. The analysis found two principal modes, one rapid and excitatory, the other slower and inhibitory. The two modes have analogies to two of the pathways in a block-structured model of the encoder that was developed from previous physiological investigations of the neuron. These results support the block-structured model and offer a new approach to identifying the components responsible for the nonlinear dynamic properties of this neuronal encoder.

[1]  V.Z. Marmarelis,et al.  Modeling of neural systems by use of neuronal modes , 1993, IEEE Transactions on Biomedical Engineering.

[2]  A S French,et al.  A nonlinear cascade model for action potential encoding in an insect sensory neuron. , 1989, Biophysical journal.

[3]  A S French,et al.  Phentolamine selectively affects the fast sodium component of sensory adaptation in an insect mechanoreceptor. , 1990, Journal of neurobiology.

[4]  A. V. Holden,et al.  The estimation of the frequency response function of a mechanoreceptor , 1972, Kybernetik.

[5]  A. S. French,et al.  The mechanosensory apparatus of the femoral tactile spine of the cockroach, Periplaneta americana , 2004, Cell and Tissue Research.

[6]  A S French,et al.  Slowly inactivating outward currents in a cuticular mechanoreceptor neuron of the cockroach (Periplaneta americana). , 1995, Journal of neurophysiology.

[7]  A. S. French.  The effects of temperature on action potential encoding in the cockroach tactile spine , 1985, Journal of Comparative Physiology A.

[8]  M. J. Korenberg,et al.  White-noise analysis of nonlinear behavior in an insect sensory neuron: Kernel and cascade approaches , 1988, Biological Cybernetics.

[9]  Andrew S. French.  Ouabain selectively affects the slow component of sensory adaptation in an insect mechanoreceptor , 1989, Brain Research.

[10]  A S French,et al.  The morphology of the sensory neuron in the cockroach femoral tactile spine. , 1993, Journal of neurophysiology.

[11]  A. S. French.  Action potential adaptation in the femoral tactile spine of the cockroach,Periplaneta americana , 1984, Journal of Comparative Physiology A.

[12]  Michael J. Korenberg,et al.  Dissection of a nonlinear cascade model for sensory encoding , 2006, Annals of Biomedical Engineering.

[13]  A S French,et al.  Intracellular measurements from a rapidly adapting sensory neuron. , 1991, Journal of neurophysiology.

[14]  V.Z. Marmarelis,et al.  Signal transformation and coding in neural systems , 1989, IEEE Transactions on Biomedical Engineering.

[15]  K. M. Chapman,et al.  A Linear Transfer Function underlying Impulse Frequency Modulation in a Cockroach Mechanoreceptor , 1963, Nature.

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

[17]  V. Marmarelis.  Identification of nonlinear biological systems using laguerre expansions of kernels , 1993, Annals of Biomedical Engineering.

[18]  J. Pringle,et al.  The Response Of A Sense Organ To A Harmonic Stimulus , 1952 .

[19]  A. S. French.  Removal of rapid sensory adaptation from an insect mechanoreceptor neuron by oxidizing agents which affect sodium channel inactivation , 1987, Journal of Comparative Physiology A.

[20]  Andrew S. French,et al.  Intracellular nonlinear frequency response measurements in the cockroach tactile spine neuron , 1991, Biological Cybernetics.

[21]  A. S. French.  Strength-duration properties of a rapidly adapting insect sensory neuron , 1986, Journal of Comparative Physiology A.

[22]  A S French,et al.  Two components of rapid sensory adaptation in a cockroach mechanoreceptor neuron. , 1989, Journal of neurophysiology.

[23]  A S French,et al.  After-hyperpolarization and receptor potential attenuation following bursts of action potentials in an insect mechanoreceptor. , 1985, Canadian journal of physiology and pharmacology.

[24]  Andrew S. French,et al.  A nonlinear model of step responses in the cockroach tactile spine neuron , 1994, Biological Cybernetics.

[25]  A. S. French.  Sensory transduction in an insect mechanoreceptor: Linear and nonlinear properties , 1980, Biological Cybernetics.