Recurrence Quantification Analysis of Spontaneous Electrophysiological Activity during Development: Characterization of In Vitro Neuronal Networks Cultured on Multi Electrode Array Chips

The combination of a nonlinear time series analysis technique, Recurrence Quantification Analysis (RQA) based on Recurrence Plots (RPs), and traditional statistical analysis for neuronal electrophysiology is proposed in this paper as an innovative paradigm for studying the variation of spontaneous electrophysiological activity of in vitro Neuronal Networks (NNs) coupled to Multielectrode Array (MEA) chips. Recurrence, determinism, entropy, distance of activity patterns, and correlation in correspondence to spike and burst parameters (e.g., mean spiking rate, mean bursting rate, burst duration, spike in burst, etc.) have been computed to characterize and assess the daily changes of the neuronal electrophysiology during neuronal network development and maturation. The results show the similarities/differences between several channels and time periods as well as the evolution of the spontaneous activity in the MEA chip. RPs could be used for graphically exploring possible neuronal dynamic breaking/changing points, whereas RQA parameters are suited for locating them. The combination of RQA with traditional approaches improves the identification, description, and prediction of electrophysiological changes and it will be used to allow intercomparison between results obtained from different MEA chips. Results suggest the proposed processing paradigm as a valuable tool to analyze neuronal activity for screening purposes (e.g., toxicology, neurodevelopmental toxicology).

[1]  Fraser,et al.  Independent coordinates for strange attractors from mutual information. , 1986, Physical review. A, General physics.

[2]  Alessandro Vato,et al.  Burst detection algorithms for the analysis of spatio-temporal patterns in cortical networks of neurons , 2005, Neurocomputing.

[3]  Jürgen Kurths,et al.  Recurrence plots for the analysis of complex systems , 2009 .

[4]  K. Muramoto,et al.  Frequency of synchronous oscillations of neuronal activity increases during development and is correlated to the number of synapses in cultured cortical neuron networks , 1993, Neuroscience Letters.

[5]  John M. Beggs,et al.  Neuronal Avalanches in Neocortical Circuits , 2003, The Journal of Neuroscience.

[6]  L. L. Bologna,et al.  Self-organization and neuronal avalanches in networks of dissociated cortical neurons , 2008, Neuroscience.

[7]  K. Gopal Neurotoxic effects of mercury on auditory cortex networks growing on microelectrode arrays: a preliminary analysis. , 2003, Neurotoxicology and teratology.

[8]  J. Zbilut,et al.  Embeddings and delays as derived from quantification of recurrence plots , 1992 .

[9]  G. Gross,et al.  Drug evaluations using neuronal networks cultured on microelectrode arrays. , 2000, Biosensors & bioelectronics.

[10]  J. Kurths,et al.  Recurrence-plot-based measures of complexity and their application to heart-rate-variability data. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[11]  H. Robinson,et al.  The mechanisms of generation and propagation of synchronized bursting in developing networks of cortical neurons , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  F. Strozzi,et al.  Recurrence quantification based Liapunov exponents for monitoring divergence in experimental data , 2002 .

[13]  Changes of the inner time structures in the sequences of interspike intervals produced by the activity of excitatory and inhibitory synapses: simulation with Gaussian input processes. , 1997, Physiological research.

[14]  G. Bi,et al.  Distributed synaptic modification in neural networks induced by patterned stimulation , 1999, Nature.

[15]  Jürgen Kurths,et al.  Influence of observational noise on the recurrence quantification analysis , 2002 .

[16]  P. S. Wolters,et al.  Longterm stability and developmental changes in spontaneous network burst firing patterns in dissociated rat cerebral cortex cell cultures on multielectrode arrays , 2004, Neuroscience Letters.

[17]  H. Robinson,et al.  Simultaneous induction of pathway-specific potentiation and depression in networks of cortical neurons. , 1999, Biophysical journal.

[18]  Remigiusz Tarnecki,et al.  Recurrence plots of neuronal spike trains , 1993, Biological Cybernetics.

[19]  Sophocles J. Orfanidis,et al.  Optimum Signal Processing: An Introduction , 1988 .

[20]  A. Giuliani,et al.  Recurrence quantification analysis of the logistic equation with transients , 1996 .

[21]  Sergio Martinoia,et al.  Neural Signal Manager: a collection of classical and innovative tools for multi‐channel spike train analysis , 2009 .

[22]  R. Kass,et al.  Multiple neural spike train data analysis: state-of-the-art and future challenges , 2004, Nature Neuroscience.

[23]  J. A. Stewart,et al.  Nonlinear Time Series Analysis , 2015 .

[24]  Steve M. Potter,et al.  An extremely rich repertoire of bursting patterns during the development of cortical cultures , 2006, BMC Neuroscience.

[25]  Shimon Marom,et al.  Development, learning and memory in large random networks of cortical neurons: lessons beyond anatomy , 2002, Quarterly Reviews of Biophysics.

[26]  Alessandro Vato,et al.  Dissociated cortical networks show spontaneously correlated activity patterns during in vitro development , 2006, Brain Research.

[27]  M. Corner,et al.  Dynamics and plasticity in developing neuronal networks in vitro. , 2005, Progress in brain research.

[28]  D. Ruelle,et al.  Recurrence Plots of Dynamical Systems , 1987 .

[29]  Masahiro Kawahara,et al.  Formation and maturation of synapses in primary cultures of rat cerebral cortical cells: an electron microscopic study , 1993, Neuroscience Research.

[30]  Paolo Massobrio,et al.  A novel algorithm for precise identification of spikes in extracellularly recorded neuronal signals , 2009, Journal of Neuroscience Methods.

[31]  M. Koebbe Use of recurrence plots in analysis of time-series data , 1992 .

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

[33]  C L Webber,et al.  Dynamical assessment of physiological systems and states using recurrence plot strategies. , 1994, Journal of applied physiology.

[34]  A. Kriegstein,et al.  Morphological classification of rat cortical neurons in cell culture , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  Dieter G Weiss,et al.  Functional screening of traditional antidepressants with primary cortical neuronal networks grown on multielectrode neurochips , 2006, The European journal of neuroscience.

[36]  G. Gross,et al.  Characterization of acute neurotoxic effects of trimethylolpropane phosphate via neuronal network biosensors. , 2001, Biosensors & bioelectronics.

[37]  Mehmet Emre Çek,et al.  Analysis of observed chaotic data , 2004 .

[38]  G Shahaf,et al.  Learning in Networks of Cortical Neurons , 2001, The Journal of Neuroscience.

[39]  M. Chiappalone,et al.  Networks of neurons coupled to microelectrode arrays: a neuronal sensory system for pharmacological applications. , 2003, Biosensors & bioelectronics.

[40]  G. Gross,et al.  Quantification of acute neurotoxic effects of trimethyltin using neuronal networks cultured on microelectrode arrays. , 2000, Neurotoxicology.

[41]  Shimon Marom,et al.  Selective Adaptation in Networks of Cortical Neurons , 2003, The Journal of Neuroscience.

[42]  H. Robinson,et al.  Modification of parallel activity elicited by propagating bursts in developing networks of rat cortical neurones , 1998, The European journal of neuroscience.

[43]  J. Kurths,et al.  Synchronization Analysis of Neuronal Networks by Means of Recurrence Plots , 2007 .

[44]  Norbert Marwan,et al.  Extended Recurrence Plot Analysis and its Application to ERP Data , 2002, Int. J. Bifurc. Chaos.

[45]  Sergio Martinoia,et al.  Connecting Neurons to a Mobile Robot: An In Vitro Bidirectional Neural Interface , 2007, Comput. Intell. Neurosci..