A method for closed-loop presentation of sensory stimuli conditional on the internal brain-state of awake animals

Brain activity often consists of interactions between internal-or on-going-and external-or sensory-activity streams, resulting in complex, distributed patterns of neural activity. Investigation of such interactions could benefit from closed-loop experimental protocols in which one stream can be controlled depending on the state of the other. We describe here methods to present rapid and precisely timed visual stimuli to awake animals, conditional on features of the animal's on-going brain state; those features are the presence, power and phase of oscillations in local field potentials (LFP). The system can process up to 64 channels in real time. We quantified its performance using simulations, synthetic data and animal experiments (chronic recordings in the dorsal cortex of awake turtles). The delay from detection of an oscillation to the onset of a visual stimulus on an LCD screen was 47.5ms and visual-stimulus onset could be locked to the phase of ongoing oscillations at any frequency ≤40Hz. Our software's architecture is flexible, allowing on-the-fly modifications by experimenters and the addition of new closed-loop control and analysis components through plugins. The source code of our system "StimOMatic" is available freely as open-source.

[1]  Burr Settles,et al.  Active Learning Literature Survey , 2009 .

[2]  Jeffrey D. Schall,et al.  Review of signal distortion through metal microelectrode recording circuits and filters , 2008, Journal of Neuroscience Methods.

[3]  N. Fisher,et al.  Statistical Analysis of Circular Data , 1993 .

[4]  Dawn M. Taylor,et al.  Direct Cortical Control of 3D Neuroprosthetic Devices , 2002, Science.

[5]  Theodore H. Bullock,et al.  Plurality of Viual Mismatch Potentials in a Reptile , 1993, Journal of Cognitive Neuroscience.

[6]  Kwabena Boahen,et al.  Space coding by gamma oscillations in the barn owl optic tectum. , 2011, Journal of neurophysiology.

[7]  Jon A. Mukand,et al.  Neuronal ensemble control of prosthetic devices by a human with tetraplegia , 2006, Nature.

[8]  Philippe Kahane,et al.  Watching brain TV and playing brain ball exploring novel BCI strategies using real-time analysis of human intracranial data. , 2009, International review of neurobiology.

[9]  Miguel A. L. Nicolelis,et al.  Real-time control of a robot arm using simultaneously recorded neurons in the motor cortex , 1999, Nature Neuroscience.

[10]  T. Hafting,et al.  Frequency of gamma oscillations routes flow of information in the hippocampus , 2009, Nature.

[11]  C. Koch,et al.  Category-specific visual responses of single neurons in the human medial temporal lobe , 2000, Nature Neuroscience.

[12]  G. Buzsáki,et al.  Selective suppression of hippocampal ripples impairs spatial memory , 2009, Nature Neuroscience.

[13]  Ryan D. Darling,et al.  Theta-contingent Trial Presentation Accelerates Learning Rate and Enhances Hippocampal Plasticity during Trace Eyeblink Conditioning , 2004 .

[14]  Tim Gollisch,et al.  Closed-Loop Measurements of Iso-Response Stimuli Reveal Dynamic Nonlinear Stimulus Integration in the Retina , 2012, Neuron.

[15]  Weiping Li,et al.  Applied Nonlinear Control , 1991 .

[16]  M. Steriade Impact of network activities on neuronal properties in corticothalamic systems. , 2001, Journal of neurophysiology.

[17]  Michael J. Goard,et al.  Basal Forebrain Activation Enhances Cortical Coding of Natural Scenes , 2009, Nature Neuroscience.

[18]  D. Kleinfeld,et al.  Visual stimuli induce waves of electrical activity in turtle cortex. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[19]  A. Grinvald,et al.  Dynamics of Ongoing Activity: Explanation of the Large Variability in Evoked Cortical Responses , 1996, Science.

[20]  Pierre Yger,et al.  Network-State Modulation of Power-Law Frequency-Scaling in Visual Cortical Neurons , 2009, PLoS Comput. Biol..

[21]  J. Prechtl,et al.  Visual motion induces synchronous oscillations in turtle visual cortex. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[22]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[23]  Samuel P. Burns,et al.  Comparisons of the Dynamics of Local Field Potential and Multiunit Activity Signals in Macaque Visual Cortex , 2010, The Journal of Neuroscience.

[24]  K. Harris,et al.  State-Dependent Representation of Amplitude-Modulated Noise Stimuli in Rat Auditory Cortex , 2011, The Journal of Neuroscience.

[25]  Ueli Rutishauser,et al.  Online detection and sorting of extracellularly recorded action potentials in human medial temporal lobe recordings, in vivo , 2006, Journal of Neuroscience Methods.

[26]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[27]  Guillaume Gibert,et al.  OpenViBE: An Open-Source Software Platform to Design, Test, and Use BrainComputer Interfaces in Real and Virtual Environments , 2010, PRESENCE: Teleoperators and Virtual Environments.

[28]  Theodore Holmes Bullock How do Brains Work? , 1993, Birkhäuser Boston.

[29]  D Kleinfeld,et al.  Direct evidence for local oscillatory current sources and intracortical phase gradients in turtle visual cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[30]  N. Birbaumer,et al.  BCI2000: a general-purpose brain-computer interface (BCI) system , 2004, IEEE Transactions on Biomedical Engineering.

[31]  Benjamin I. Rapoport,et al.  Real-Time Brain Oscillation Detection and Phase-Locked Stimulation Using Autoregressive Spectral Estimation and Time-Series Forward Prediction , 2013, IEEE Transactions on Biomedical Engineering.

[32]  C. Koch,et al.  Invariant visual representation by single neurons in the human brain , 2005, Nature.

[33]  Justin C. Williams,et al.  Chronic neural recording using silicon-substrate microelectrode arrays implanted in cerebral cortex , 2004, IEEE Transactions on Biomedical Engineering.

[34]  Christof Koch,et al.  Human Neuroscience , 2022 .

[35]  L. Frank,et al.  Awake Hippocampal Sharp-Wave Ripples Support Spatial Memory , 2012, Science.

[36]  Partha P. Mitra,et al.  Sampling Properties of the Spectrum and Coherency of Sequences of Action Potentials , 2000, Neural Computation.

[37]  Joyce Keifer,et al.  Thalamocortical Connections in the Pond Turtle Pseudemys scripta elegans , 2005, Brain, Behavior and Evolution.

[38]  T H Bullock,et al.  Event-related potentials to omitted visual stimuli in a reptile. , 1994, Electroencephalography and clinical neurophysiology.

[39]  R. Normann,et al.  A method for pneumatically inserting an array of penetrating electrodes into cortical tissue , 2006, Annals of Biomedical Engineering.

[40]  C. Pavlides,et al.  Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. , 1988, Brain research.

[41]  T. Poggio,et al.  Object Selectivity of Local Field Potentials and Spikes in the Macaque Inferior Temporal Cortex , 2006, Neuron.

[42]  R. Shapley,et al.  Is Gamma-Band Activity in the Local Field Potential of V1 Cortex a “Clock” or Filtered Noise? , 2011, The Journal of Neuroscience.

[43]  E. Fetz Operant Conditioning of Cortical Unit Activity , 1969, Science.

[44]  C. Koch,et al.  A category-specific response to animals in the right human amygdala , 2011, Nature Neuroscience.

[45]  T. Bullock How do Brains Work?: Papers of a Comparative Neurophysiologist , 1993 .

[46]  Bruce S. Davie,et al.  Computer Networks: A Systems Approach , 1996 .

[47]  N. Logothetis,et al.  Very slow activity fluctuations in monkey visual cortex: implications for functional brain imaging. , 2003, Cerebral cortex.

[48]  C. Gray,et al.  Cellular Mechanisms Contributing to Response Variability of Cortical Neurons In Vivo , 1999, The Journal of Neuroscience.

[49]  Philipp Berens,et al.  CircStat: AMATLABToolbox for Circular Statistics , 2009, Journal of Statistical Software.

[50]  A. Reiner,et al.  A stereotaxic atlas of the forebrain and midbrain of the eastern painted turtle (Chrysemys picta picta). , 1980, Journal fur Hirnforschung.

[51]  Stephen Travis Pope,et al.  A cookbook for using the model-view controller user interface paradigm in Smalltalk-80 , 1988 .

[52]  G. Horwitz,et al.  Nonlinear analysis of macaque V1 color tuning reveals cardinal directions for cortical color processing , 2012, Nature Neuroscience.

[53]  T H Bullock,et al.  Barbiturate sensitive components of visual ERPs in a reptile. , 1992, Neuroreport.

[54]  Xing Dajun,et al.  Searching for Autocoherence in the Cortical Network with a Time-Frequency Analysis of the Local Field Potential , 2008 .

[55]  Philip S. Ulinski,et al.  The Cerebral Cortex of Reptiles , 1990 .

[56]  U. Rutishauser,et al.  Learning and Representation of Declarative Memories by Single Neurons in the Human Brain , 2008 .

[57]  Kristin N. Mauldin,et al.  Nonpharmacological amelioration of age-related learning deficits: the impact of hippocampal theta-triggered training. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[58]  Alan Peters,et al.  Comparative structure and evolution of cerebral cortex , 1990 .

[59]  Wilson S. Geisler,et al.  Gaze-contingent real-time simulation of arbitrary visual fields , 2002, IS&T/SPIE Electronic Imaging.

[60]  C. Pavlides,et al.  Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of θ-rhythm , 1988, Brain Research.

[61]  M. Wilson,et al.  Disruption of ripple‐associated hippocampal activity during rest impairs spatial learning in the rat , 2009, Hippocampus.

[62]  Eun Jung Hwang,et al.  Brain Control of Movement Execution Onset Using Local Field Potentials in Posterior Parietal Cortex , 2009, The Journal of Neuroscience.

[63]  E. Fetz,et al.  Direct control of paralyzed muscles by cortical neurons , 2008, Nature.

[64]  Tobias Elze,et al.  Achieving precise display timing in visual neuroscience experiments , 2010, Journal of Neuroscience Methods.

[65]  Partha P. Mitra,et al.  Observed Brain Dynamics , 2007 .