Irregular Firing of Isolated Cortical Interneurons in Vitro Driven by Intrinsic Stochastic Mechanisms

Pharmacologically isolated GABAergic irregular spiking and stuttering interneurons in the mouse visual cortex display highly irregular spike times, with high coefficients of variation 0.93, in response to a depolarizing, constant current input. This is in marked contrast to cortical pyramidal cells, which spike quite regularly in response to the same current injection. We applied time-series analysis methods to show that the irregular behavior of the interneurons was not a consequence of low-dimensional, deterministic processes. These methods were also applied to the Hindmarsh and Rose neuronal model to confirm that the methods are adequate for the types of data under investigation. This result has important consequences for the origin of fluctuations observed in the cortex in vivo.

[1]  Hatsuo Hayashi,et al.  Chaos in the self-sustained oscillation of an excitable biological membrane under sinusoidal stimulation , 1982 .

[2]  A. N. Sharkovskiĭ Dynamic systems and turbulence , 1989 .

[3]  Jianfeng Feng,et al.  Significance of random neuronal drive , 2001, Neurocomputing.

[4]  M. C. Angulo,et al.  Molecular and Physiological Diversity of Cortical Nonpyramidal Cells , 1997, The Journal of Neuroscience.

[5]  T. Sauer,et al.  Correlation dimension of attractors through interspike intervals , 1997 .

[6]  H. Abarbanel,et al.  Determining embedding dimension for phase-space reconstruction using a geometrical construction. , 1992, Physical review. A, Atomic, molecular, and optical physics.

[7]  J. Rinzel,et al.  Bursting, beating, and chaos in an excitable membrane model. , 1985, Biophysical journal.

[8]  Holger Kantz,et al.  Practical implementation of nonlinear time series methods: The TISEAN package. , 1998, Chaos.

[9]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1990 .

[10]  Jaeseung Jeong,et al.  Dynamical Heterogeneity of Suprachiasmatic Nucleus Neurons Based on Regularity and Determinism , 2005, Journal of Computational Neuroscience.

[11]  Hatsuo Hayashi,et al.  Transition to chaos via intermittency in the onchidium pacemaker neuron , 1983 .

[12]  J. Rossier,et al.  Classification of fusiform neocortical interneurons based on unsupervised clustering. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[13]  J. Rossier,et al.  Properties of bipolar VIPergic interneurons and their excitation by pyramidal neurons in the rat neocortex , 1998, The European journal of neuroscience.

[14]  S. T. Kitai,et al.  Firing patterns and synaptic potentials of identified giant aspiny interneurons in the rat neostriatum , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  Charles J. Wilson,et al.  Synaptic Regulation of Action Potential Timing in Neostriatal Cholinergic Interneurons , 1998, The Journal of Neuroscience.

[16]  T. Schreiber,et al.  Surrogate time series , 1999, chao-dyn/9909037.

[17]  André Longtin,et al.  Interspike interval attractors from chaotically driven neuron models , 1997 .

[18]  H. Kantz,et al.  Nonlinear time series analysis , 1997 .

[19]  Y. Kawaguchi Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  Y. Kawaguchi,et al.  Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex. , 1993, Journal of neurophysiology.

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

[22]  H. Markram,et al.  Interneurons of the neocortical inhibitory system , 2004, Nature Reviews Neuroscience.

[23]  B. Connors,et al.  The Spatial Dimensions of Electrically Coupled Networks of Interneurons in the Neocortex , 2002, The Journal of Neuroscience.

[24]  G. Tamás,et al.  Cholinergic activation and tonic excitation induce persistent gamma oscillations in mouse somatosensory cortex in vitro , 1998, The Journal of physiology.

[25]  W. J. Nowack Methods in Neuronal Modeling , 1991, Neurology.

[26]  André Longtin,et al.  NONLINEAR FORECASTING OF SPIKE TRAINS FROM SENSORY NEURONS , 1993 .

[27]  H. Markram,et al.  Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. , 2000, Science.

[28]  A. Destexhe,et al.  The high-conductance state of neocortical neurons in vivo , 2003, Nature Reviews Neuroscience.

[29]  C. Canavier,et al.  Scaling of prediction error does not confirm chaotic dynamics underlying irregular firing using interspike intervals from midbrain dopamine neurons , 2004, Neuroscience.

[30]  J. Hindmarsh,et al.  A model of neuronal bursting using three coupled first order differential equations , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[31]  H. Markram,et al.  Correlation maps allow neuronal electrical properties to be predicted from single-cell gene expression profiles in rat neocortex. , 2004, Cerebral cortex.

[32]  Henry D. I. Abarbanel,et al.  Analysis of Observed Chaotic Data , 1995 .

[33]  O. Paulsen,et al.  Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro , 1998, Nature.

[34]  Y. Kubota,et al.  Physiological and morphological identification of somatostatin- or vasoactive intestinal polypeptide-containing cells among GABAergic cell subtypes in rat frontal cortex , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  F. Takens Detecting strange attractors in turbulence , 1981 .

[36]  Alan Garfinkel,et al.  Period-doubling bifurcation in an array of coupled stochastically excitable elements subjected to global periodic forcing. , 2009, Physical review letters.

[37]  T. Sejnowski,et al.  Reliability of spike timing in neocortical neurons. , 1995, Science.

[38]  Idan Segev,et al.  Methods in Neuronal Modeling , 1988 .

[39]  Charles J. Wilson,et al.  Spontaneous Activity of Neostriatal Cholinergic Interneurons In Vitro , 1999, The Journal of Neuroscience.

[40]  Farmer,et al.  Predicting chaotic time series. , 1987, Physical review letters.

[41]  Hatsuo Hayashi,et al.  Chaotic behavior in the Onchidium giant neuron under sinusoidal stimulation , 1982 .

[42]  Peter F. Rowat,et al.  Interspike Interval Statistics in the Stochastic Hodgkin-Huxley Model: Coexistence of Gamma Frequency Bursts and Highly Irregular Firing , 2007, Neural Computation.

[43]  H. Akaike A new look at the statistical model identification , 1974 .

[44]  K. Doya,et al.  Chaos may enhance information transmission in the inferior olive. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[45]  B. Hille,et al.  Ionic channels of excitable membranes , 2001 .

[46]  J. Byrne,et al.  Routes to chaos in a model of a bursting neuron. , 1990, Biophysical journal.

[47]  James Theiler,et al.  Testing for nonlinearity in time series: the method of surrogate data , 1992 .

[48]  Charles J. Wilson,et al.  Intrinsic Membrane Properties Underlying Spontaneous Tonic Firing in Neostriatal Cholinergic Interneurons , 2000, The Journal of Neuroscience.

[49]  D C Spray,et al.  How to close a gap junction channel. Efficacies and potencies of uncoupling agents. , 2001, Methods in molecular biology.

[50]  Y. Kawaguchi,et al.  Parvalbumin, somatostatin and cholecystokinin as chemical markers for specific GABAergic interneuron types in the rat frontal cortex , 2002, Journal of neurocytology.

[51]  H. Kantz,et al.  Embedding of sequences of time intervals , 1997 .