Consistent dynamics suggests tight regulation of biophysical parameters in a small network of bursting neurons.

The neuronal firing patterns in the pyloric network of crustaceans are remarkably consistent among animals. Although this characteristic of the pyloric network is well-known, the biophysical mechanisms underlying the regulation of the systems output are receiving renewed attention. Computer simulations of the pyloric network recently demonstrated that consistent motor output can be achieved from neurons with disparate biophysical parameters among animals. Here we address this hypothesis by pharmacologically manipulating the pyloric network and analyzing the emerging voltage oscillations and firing patterns. Our results show that the pyloric network of the lobster stomatogastric ganglion maintains consistent and regular firing patterns even when entire populations of specific voltage-gated channels and synaptic receptors are blocked. The variations of temporal parameters used to characterize the burst patterns of the neurons as well as their intraburst spike dynamics do not display statistically significant increase after blocking the transient K-currents (with 4-aminopyridine), the glutamatergic inhibitory synapses (with picrotoxin), or the cholinergic synapses (with atropine) in pyloric networks from different animals. These data suggest that in this very compact circuit, the biophysical parameters are cell-specific and tightly regulated.

[1]  E. Marder,et al.  Variable channel expression in identified single and electrically coupled neurons in different animals , 2006, Nature Neuroscience.

[2]  P. Meyrand,et al.  Long-term expression of two interacting motor pattern-generating networks in the stomatogastric system of freely behaving lobster. , 1998, Journal of Neurophysiology.

[3]  Arthur C. Sanderson,et al.  Sequential interval histogram analysis of non-stationary neuronal spike trains , 1976, Biological Cybernetics.

[4]  E Marder,et al.  Modulation of Oscillator Interactions in the Crab Stomatogastric Ganglion by Crustacean Cardioactive Peptide , 1997, The Journal of Neuroscience.

[5]  Yair Manor,et al.  Synaptic depression in conjunction with A-current channels promote phase constancy in a rhythmic network. , 2005, Journal of neurophysiology.

[6]  Brian Mulloney,et al.  Organization of the stomatogastric ganglion of the spiny lobster , 2004, Journal of comparative physiology.

[7]  Bruce R. Johnson,et al.  Activity-Independent Homeostasis in Rhythmically Active Neurons , 2003, Neuron.

[8]  E. Marder,et al.  Ionic currents of the lateral pyloric neuron of the stomatogastric ganglion of the crab. , 1992, Journal of neurophysiology.

[9]  A. Selverston A Neural Infrastructure for Rhythmic Motor Patterns , 2005, Cellular and Molecular Neurobiology.

[10]  Jeffrey B. Thuma,et al.  Quantification of cardiac sac network effects on a movement-related parameter of pyloric network output in the lobster. , 2002, Journal of neurophysiology.

[11]  Scott L. Hooper,et al.  Lobster (Panulirus interruptus) Pyloric Muscles Express the Motor Patterns of Three Neural Networks, Only One of Which Innervates the Muscles , 2003, The Journal of Neuroscience.

[12]  R. Harris-Warrick,et al.  Aminergic modulation in lobster stomatogastric ganglion. I. Effects on motor pattern and activity of neurons within the pyloric circuit. , 1986, Journal of neurophysiology.

[13]  R. Harris-Warrick,et al.  Physiological role of the transient potassium current in the pyloric circuit of the lobster stomatogastric ganglion. , 1992, Journal of neurophysiology.

[14]  M Bidaut,et al.  Pharmacological dissection of pyloric network of the lobster stomatogastric ganglion using picrotoxin. , 1980, Journal of neurophysiology.

[15]  R. Harris-Warrick,et al.  Distributed Effects of Dopamine Modulation in the Crustacean Pyloric Network a , 1998, Annals of the New York Academy of Sciences.

[16]  Michael J. Berry,et al.  A test of metabolically efficient coding in the retina , 2002, Network.

[17]  Mikhail I. Rabinovich,et al.  Self-regularization of chaos in neural systems: experimental and theoretical results , 1997 .

[18]  R. Harris-Warrick,et al.  Modulation of neural networks for behavior. , 1991, Annual review of neuroscience.

[19]  E. Marder,et al.  Activity-Dependent Regulation of Potassium Currents in an Identified Neuron of the Stomatogastric Ganglion of the Crab Cancer borealis , 1999, The Journal of Neuroscience.

[20]  E. Marder,et al.  Similar network activity from disparate circuit parameters , 2004, Nature Neuroscience.

[21]  Eve Marder,et al.  Cellular, synaptic and network effects of neuromodulation , 2002, Neural Networks.

[22]  E. Marder,et al.  A Model Neuron with Activity-Dependent Conductances Regulated by Multiple Calcium Sensors , 1998, The Journal of Neuroscience.

[23]  Thierry Bal,et al.  The pyloric central pattern generator in Crustacea: a set of conditional neuronal oscillators , 1988, Journal of Comparative Physiology A.

[24]  Jeffrey B. Thuma,et al.  Quantification of gastric mill network effects on a movement related parameter of pyloric network output in the lobster. , 2002, Journal of neurophysiology.

[25]  D K Hartline,et al.  Effects of soma isolation on outward currents measured under voltage clamp in spiny lobster stomatogastric motor neurons. , 1993, Journal of neurophysiology.

[26]  Allen I. Selverston,et al.  Organization of the stomatogastric ganglion of the spiny lobster , 2004, Journal of comparative physiology.

[27]  A. Bulloch,et al.  Stability and variability of synapses in the adult molluskan CNS. , 2000, Journal of neurobiology.

[28]  Katherine Graubard,et al.  Voltage clamp analysis of intact stomatogastric neurons , 1991, Brain Research.

[29]  R. Harris-Warrick,et al.  Aminergic modulation in lobster stomatogastric ganglion. II. Target neurons of dopamine, octopamine, and serotonin within the pyloric circuit. , 1986, Journal of neurophysiology.

[30]  E. Marder,et al.  Failure of averaging in the construction of a conductance-based neuron model. , 2002, Journal of neurophysiology.

[31]  E Marder,et al.  Modulators with Convergent Cellular Actions Elicit Distinct Circuit Outputs , 2001, The Journal of Neuroscience.

[32]  W. Moody,et al.  Na+ channel mis‐expression accelerates K+ channel development in embryonic Xenopus laevis skeletal muscle. , 1994, The Journal of physiology.

[33]  R. Harris-Warrick,et al.  Distributed amine modulation of graded chemical transmission in the pyloric network of the lobster stomatogastric ganglion. , 1995, Journal of neurophysiology.

[34]  R. Harris-Warrick,et al.  Dopamine modulates two potassium currents and inhibits the intrinsic firing properties of an identified motor neuron in a central pattern generator network. , 1999, Journal of neurophysiology.

[35]  R. Harris-Warrick,et al.  Amine modulation of the transient potassium current in identified cells of the lobster stomatogastric ganglion. , 2001, Journal of neurophysiology.

[36]  R. D. Pinto,et al.  Synaptic modulation of the interspike interval signatures of bursting pyloric neurons. , 2003, Journal of neurophysiology.

[37]  R. Nargeot,et al.  Voltage-Dependent Switching of Sensorimotor Integration by a Lobster Central Pattern Generator , 2003, The Journal of Neuroscience.

[38]  R. Harris-Warrick,et al.  Dopamine modulation of two delayed rectifier potassium currents in a small neural network. , 2005, Journal of neurophysiology.

[39]  Adelbert Ames,et al.  CNS energy metabolism as related to function , 2000, Brain Research Reviews.

[40]  R Huerta,et al.  Dynamic control of irregular bursting in an identified neuron of an oscillatory circuit. , 1999, Journal of neurophysiology.

[41]  D. F. Russell,et al.  Slow active potentials and bursting motor patterns in pyloric network of the lobster, Panulirus interruptus. , 1982, Journal of neurophysiology.

[42]  M. Wong-Riley Cytochrome oxidase: an endogenous metabolic marker for neuronal activity , 1989, Trends in Neurosciences.

[43]  Bruce R. Johnson,et al.  Dopamine modulation of calcium currents in pyloric neurons of the lobster stomatogastric ganglion. , 2003, Journal of neurophysiology.

[44]  Eve Marder,et al.  Animal-to-Animal Variability in Motor Pattern Production in Adults and during Growth , 2005, The Journal of Neuroscience.

[45]  Attila Szücs,et al.  Dopamine modulation of spike dynamics in bursting neurons , 2005, The European journal of neuroscience.

[46]  S. Gueron,et al.  Dopamine modulation of two subthreshold currents produces phase shifts in activity of an identified motoneuron. , 1995, Journal of neurophysiology.

[47]  A. Selverston,et al.  Organization of the stomatogastric ganglion of the spiny lobster , 2004, Journal of comparative physiology.

[48]  E. Marder,et al.  Transmitter identification of pyloric neurons: electrically coupled neurons use different transmitters. , 1984, Journal of neurophysiology.