Effects of random external background stimulation on network synaptic stability after tetanization

We constructed a simulated spiking neural network model to investigate the effects of random background stimulation on the dynamics of network activity patterns and tetanus induced network plasticity. The simulated model was a “leaky integrate-and-fire” (LIF) neural model with spike-timing-dependent plasticity (STDP) and frequency-dependent synaptic depression. Spontaneous and evoked activity patterns were compared with those of living neuronal networks cultured on multielectrode arrays. To help visualize activity patterns and plasticity in our simulated model, we introduced new population measures called Center of Activity (CA) and Center of Weights (CW) to describe the spatio-temporal dynamics of network-wide firing activity and network-wide synaptic strength, respectively. Without random background stimulation, the network synaptic weights were unstable and often drifted after tetanization. In contrast, with random background stimulation, the network synaptic weights remained close to their values immediately after tetanization. The simulation suggests that the effects of tetanization on network synaptic weights were difficult to control because of ongoing synchronized spontaneous bursts of action potentials, or “barrages.” Random background stimulation helped maintain network synaptic stability after tetanization by reducing the number and thus the influence of spontaneous barrages. We used our simulated network to model the interaction between ongoing neural activity, external stimulation and plasticity, and to guide our choice of sensory-motor mappings for adaptive behavior in hybrid neural-robotic systems or “hybrots.”

[1]  G. Edelman,et al.  Spike-timing dynamics of neuronal groups. , 2004, Cerebral cortex.

[2]  H. Markram,et al.  Information Processing with Frequency-Dependent Synaptic Connections , 1998, Neurobiology of Learning and Memory.

[3]  Steve M. Potter,et al.  Removing Some 'A' from AI: Embodied Cultured Networks , 2003, Embodied Artificial Intelligence.

[4]  Henry Markram,et al.  Computer models and analysis tools for neural microcircuits , 2003 .

[5]  L. Abbott,et al.  Competitive Hebbian learning through spike-timing-dependent synaptic plasticity , 2000, Nature Neuroscience.

[6]  C. McIntyre,et al.  Extracellular stimulation of central neurons: influence of stimulus waveform and frequency on neuronal output. , 2002, Journal of neurophysiology.

[7]  Steve M. Potter,et al.  A new approach to neural cell culture for long-term studies , 2001, Journal of Neuroscience Methods.

[8]  R. Caminiti,et al.  Shift of preferred directions of premotor cortical cells with arm movements performed across the workspace , 2004, Experimental Brain Research.

[9]  Guenter W. Gross,et al.  Origins of Activity Patterns in Self-Organizing Neuronal Networks in Vitro. , 1999 .

[10]  Steve M. Potter,et al.  Multi-site two-photon imaging of neurons on multi-electrode arrays , 2001 .

[11]  S.M. Potter,et al.  Spontaneous bursts are better indicators of tetanus-induced plasticity than responses to probe stimuli , 2005, Conference Proceedings. 2nd International IEEE EMBS Conference on Neural Engineering, 2005..

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

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

[14]  Yuji Ikegaya,et al.  Synfire Chains and Cortical Songs: Temporal Modules of Cortical Activity , 2004, Science.

[15]  Yan Wu,et al.  Multisite two-photon imaging of neurons on multielectrode arrays , 2001, SPIE BiOS.

[16]  Aude Billard,et al.  From Animals to Animats , 2004 .

[17]  Eshel Ben-Jacob,et al.  Generic modeling of chemotactic based self-wiring of neural networks , 1998, Neural Networks.

[18]  Sethu Vijayakumar,et al.  Adaptive Optimal Control for Redundantly Actuated Arms , 2008, SAB.

[19]  A. Georgopoulos Population activity in the control of movement. , 1994, International review of neurobiology.

[20]  Daniel A. Wagenaar,et al.  Closing the Loop: Stimulation Feedback Systems for Embodied MEA Cultures , 2006 .

[21]  Rodney A. Brooks,et al.  Cambrian Intelligence: The Early History of the New AI , 1999 .

[22]  Jean-Arcady Meyer,et al.  From Animals to Animats: Proceedings of The First International Conference on Simulation of Adaptive Behavior (Complex Adaptive Systems) , 1990 .

[23]  Daniel A. Wagenaar,et al.  The Neurally Controlled Animat: Biological Brains Acting with Simulated Bodies , 2001, Auton. Robots.

[24]  H. Robinson,et al.  Spontaneous periodic synchronized bursting during formation of mature patterns of connections in cortical cultures , 1996, Neuroscience Letters.

[25]  Olaf Sporns,et al.  Selectionism and the brain , 1994 .

[26]  Bijan Pesaran,et al.  Temporal structure in neuronal activity during working memory in macaque parietal cortex , 2000, Nature Neuroscience.

[27]  D. Linden,et al.  Long-term synaptic depression in the mammalian brain , 1994, Neuron.

[28]  Yasuhiko Jimbo,et al.  Activity-dependent enhancement in the reliability of correlated spike timings in cultured cortical neurons , 1999, Biological Cybernetics.

[29]  Kohyu Fukunishi,et al.  Dendrite classification in rat hippocampal neurons according to signal propagation properties Observation by multichannel optical recording in cultured neuronal networks , 1998, Experimental Brain Research.

[30]  G. Gross,et al.  Stimulation of monolayer networks in culture through thin-film indium-tin oxide recording electrodes , 1993, Journal of Neuroscience Methods.

[31]  Steve M. Potter,et al.  Controlling Bursting in Cortical Cultures with Closed-Loop Multi-Electrode Stimulation , 2005, The Journal of Neuroscience.

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

[33]  Eshel Ben-Jacob,et al.  Functional holography of recorded neuronal networks activity , 2007, Neuroinformatics.

[34]  John Hallam,et al.  From Animals to Animats 10 , 2008 .

[35]  Komal Rambani,et al.  Custom-made multiphoton microscope for long-term imaging of neuronal cultures to explore structural and functional plasticity , 2005, SPIE BiOS.

[36]  C. Shatz,et al.  Transient period of correlated bursting activity during development of the mammalian retina , 1993, Neuron.

[37]  B. Richmond,et al.  Intrinsic dynamics in neuronal networks. II. experiment. , 2000, Journal of neurophysiology.

[38]  Stewart W. Wilson,et al.  From Animals to Animats 5. Proceedings of the Fifth International Conference on Simulation of Adaptive Behavior , 1997 .

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

[40]  T. Bliss,et al.  A synaptic model of memory: long-term potentiation in the hippocampus , 1993, Nature.

[41]  Steve M. Potter,et al.  Effective parameters for stimulation of dissociated cultures using multi-electrode arrays , 2004, Journal of Neuroscience Methods.

[42]  Donald W. Bouldin,et al.  A Cluster Separation Measure , 1979, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[43]  T. Bliss,et al.  Long‐lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path , 1973, The Journal of physiology.

[44]  John M. Beggs,et al.  Behavioral / Systems / Cognitive Neuronal Avalanches Are Diverse and Precise Activity Patterns That Are Stable for Many Hours in Cortical Slice Cultures , 2004 .

[45]  Steve M. Potter,et al.  c 5 D ) Animat in a Petri Dish : Cultured Neural Networks for Studying Neural Computation , 2022 .

[46]  Steve M. Potter,et al.  A versatile all-channel stimulator for electrode arrays, with real-time control , 2004, Journal of neural engineering.

[47]  Guenter W. Gross,et al.  DYNAMICS OF BURST PATTERNS GENERATED BY MONOLAYER NETWORKS IN CULTURE , 1993 .

[48]  W. M. Keck,et al.  Machine Psychology : Autonomous Behavior , Perceptual Categorization and Conditioning in a Brain-based Device , 2002 .

[49]  Steve M. Potter,et al.  Two-photon Microscopy for 4D Imaging of Living Neurons , 2000 .