A Novel Bursting Mechanism of Type A Neurons in Injured Dorsal Root Ganglia

Using intracellular recording in vivo, the bursting behaviors were investigated in the neurons of chronically compressed dorsal root ganglia of the adult rat. In most cases, the first spike of a burst emerged from amplitude-increasing damped subthreshold membrane potential oscillation (SMPO) and the discharge terminated by an amplitude-decreasing damped SMPO. The rhythms of these bursting behaviors are all irregular. Since some researchers found that the stochastic dynamics can also produce similar bursting pattern, the deterministic dynamics of interevent interval (IEI) series obtained from raw membrane potential recording was detected by extraction of the hierarchy of unstable periodic orbits (UPOs) in the windowed IEI series. The results showed a number of statistically significant UPOs of order-one, order-two, and order-three. These orbits form a complex but predictable lattice of regions in which the dynamics of the bursting occurrence is deterministic. Based on a complete classification scheme, the investigated bursting can be depicted by the elliptic bursting dynamics. The significance of the finding that a neuron in the injured dorsal root ganglion has such dynamics is also discussed.

[1]  M. Devor,et al.  Spinal nerve injury enhances subthreshold membrane potential oscillations in DRG neurons: relation to neuropathic pain. , 2000, Journal of neurophysiology.

[2]  C. Morris,et al.  Voltage oscillations in the barnacle giant muscle fiber. , 1981, Biophysical journal.

[3]  J. Xing,et al.  An experimental model for chronic compression of dorsal root ganglion produced by intervertebral foramen stenosis in the rat , 1998, Pain.

[4]  Celso Grebogi,et al.  Extracting unstable periodic orbits from chaotic time series data , 1997 .

[5]  A Garfinkel,et al.  Evidence for a novel bursting mechanism in rodent trigeminal neurons. , 1998, Biophysical journal.

[6]  Eugene M. Izhikevich,et al.  Neural excitability, Spiking and bursting , 2000, Int. J. Bifurc. Chaos.

[7]  Eugene M. Izhikevich,et al.  Resonate-and-fire neurons , 2001, Neural Networks.

[8]  M. Devor,et al.  Oscillatory mechanism in primary sensory neurones. , 2002, Brain : a journal of neurology.

[9]  V I Nekorkin,et al.  Spiking behavior in a noise-driven system combining oscillatory and excitatory properties. , 2001, Physical review letters.

[10]  Grebogi,et al.  Detecting unstable periodic orbits in chaotic experimental data. , 1996, Physical review letters.

[11]  S J Schiff,et al.  Periodic orbits: a new language for neuronal dynamics. , 1998, Biophysical journal.

[12]  Eugene M. Izhikevich,et al.  Subcritical Elliptic Bursting of Bautin Type , 1999, SIAM J. Appl. Math..

[13]  K. H. Britten,et al.  Power spectrum analysis of bursting cells in area MT in the behaving monkey , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  M. Devor Pathophysiology of damaged nerves in relation to chronic pain , 1999 .

[15]  Frank C. Hoppensteadt,et al.  Bursts as a unit of neural information: selective communication via resonance , 2003, Trends in Neurosciences.

[16]  I. Pose,et al.  Oscillatory membrane potential activity in the soma of a primary afferent neuron. , 1999, Journal of neurophysiology.

[17]  S. Waxman,et al.  Subthreshold oscillations induced by spinal nerve injury in dissociated muscle and cutaneous afferents of mouse DRG. , 2002, Journal of neurophysiology.

[18]  M. Devor,et al.  Burst discharge in primary sensory neurons: triggered by subthreshold oscillations, maintained by depolarizing afterpotentials. , 2002, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  Huaguang Gu,et al.  Experimental observation of the stochastic bursting caused by coherence resonance in a neural pacemaker , 2002, Neuroreport.

[20]  Y. Wan,et al.  Subthreshold membrane oscillations underlying integer multiples firing from injured sensory neurons , 2001, Neuroreport.

[21]  J. Xing,et al.  Subthreshold membrane potential oscillations of type A neurons in injured DRG , 2001, Brain Research.

[22]  J. White,et al.  A bifurcation analysis of neuronal subthreshold oscillations. , 1995, Biophysical journal.

[23]  M. Devor,et al.  Burst Discharge in Primary Sensory Neurons: Triggered by Subthreshold Oscillations, Maintained by Depolarizing Afterpotentials , 2002, The Journal of Neuroscience.

[24]  S. H. Chandler,et al.  Membrane Resonance and Subthreshold Membrane Oscillations in Mesencephalic V Neurons: Participants in Burst Generation , 2001, The Journal of Neuroscience.

[25]  Zhuoqin Yang,et al.  Integer multiple spiking in the stochastic Chay model and its dynamical generation mechanism , 2002 .

[26]  Sauer,et al.  Reconstruction of dynamical systems from interspike intervals. , 1994, Physical review letters.

[27]  J Theiler,et al.  Two tools to test time series data for evidence of chaos and/or nonlinearity , 1994, Integrative physiological and behavioral science : the official journal of the Pavlovian Society.

[28]  R. LaMotte,et al.  Mechanical and thermal hyperalgesia and ectopic neuronal discharge after chronic compression of dorsal root ganglia. , 1999, Journal of neurophysiology.