Temporal Scales of Cortical Interactions

Higher brain functions are attributed to the cortex. Over the years it became clear that information is encoded not only in the responses of individual neurons but also in the joint activity of populations of neurons. Based on theoretical studies it has been proposed that the temporally coordinated spiking activity of many neurons is a relevant variable for information processing (VON DER MALSBURG 1981, ABELES 1982b) and that cortical neurons organize dynamically into coherent functional groups (»cell assemblies«, HEBB 1949) that are distinguished by the coordinated activity of the participating neurons. Our research focuses on the development of analysis strategies for the identification of neuronal interactions and assembly activity. We attempt to decipher the spatial and temporal scales of dynamical neuronal interactions, and their relations to the external world (stimuli and/or behavior). In order to identify neuronal assemblies, simultaneously recorded neuronal spiking activity needs to be analyzed with respect to temporal structure. To that end we developed the »unitary event« analysis method (GRUN et al. 2002a, GRUN et al. 2002b) that detects the presence of conspicuous spike coincidences and evaluates their statistical significance. The analysis of simultaneously recorded neuronal activity in monkey primary motor and frontal cortex uncovered context-dependent, rapid changes in the patterns of coincident spike activity during performance of a delayed-pointing task (RIEHLE et al. 1997) or a delayed localization task (VAADIA et al. 1989, AERTSEN et al. 1991, VAADIA et al. 1991), respectively. Spike synchronization occurred accompanied by discharge rate modulations and in the absence of spike rate modulations depending on the details of the experimental protocol. The temporal precision of such synchronized events is in the range of a few ms (GRUN et al. 1999). Data suggest that the composition of significant coincidence patterns changes depending on the computational demands (GRUN et al. 2002b), which may be taken as an indication that different assemblies are activated in relation to behavior. In the unitary event analysis a number of different time scales have to be considered and affect different parameters of the signal. Here we specifically address the different temporal scales and give interpretations in respect to the dynamics of the neuronal processes.

[1]  K A Martin,et al.  A brief history of the "feature detector". , 1994, Cerebral cortex.

[2]  H. Barlow The Biological Role of Neocortex , 1992 .

[3]  A. Aertsen,et al.  Response synchronization in the visual cortex , 1993, Current Opinion in Neurobiology.

[4]  A. Aertsen,et al.  Spike synchronization and rate modulation differentially involved in motor cortical function. , 1997, Science.

[5]  Marvin Minsky,et al.  Perceptrons: An Introduction to Computational Geometry , 1969 .

[6]  M. Abeles,et al.  Multispike train analysis , 1977, Proceedings of the IEEE.

[7]  A Aertsen,et al.  Neural dynamics in cortical networks--precision of joint-spiking events. , 2001, Novartis Foundation symposium.

[8]  S. Kaplan The Physiology of Thought , 1950 .

[9]  G. Palm Evidence, information, and surprise , 1981, Biological Cybernetics.

[10]  A. Riehle,et al.  Precise spike synchronization in monkey motor cortex involved in preparation for movement , 1999, Experimental Brain Research.

[11]  A. Aertsen,et al.  Dynamics of neuronal interactions in monkey cortex in relation to behavioural events , 1995, Nature.

[12]  M. Laubach,et al.  Cortical ensemble activity increasingly predicts behaviour outcomes during learning of a motor task , 2022 .

[13]  Stefan Rotter,et al.  Statistical Significance of Coincident Spikes: Count-Based Versus Rate-Based Statistics , 2002, Neural Computation.

[14]  E E Fetz,et al.  Temporal Coding in Neural Populations? , 1997, Science.

[15]  J J Hopfield,et al.  Neural networks and physical systems with emergent collective computational abilities. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[16]  M. Abeles The Quantification and Graphic Display of Correlations Among Three Spike Trains , 1983, IEEE Transactions on Biomedical Engineering.

[17]  Richard Passingham,et al.  Information about movements in monkeys (Macaca mulatta) with lesions of dorsal prefrontal cortex , 1978, Brain Research.

[18]  J Bullier,et al.  Structural basis of cortical synchronization. II. Effects of cortical lesions. , 1995, Journal of neurophysiology.

[19]  James L. McClelland,et al.  Parallel distributed processing: explorations in the microstructure of cognition, vol. 1: foundations , 1986 .

[20]  C. Sherrington Integrative Action of the Nervous System , 1907 .

[21]  Sonja Grün,et al.  Unitary Events in Multiple Single-Neuron Spiking Activity: I. Detection and Significance , 2002, Neural Computation.

[22]  Sonja Grün,et al.  Effect of cross-trial nonstationarity on joint-spike events , 2003, Biological Cybernetics.

[23]  E. Fetz,et al.  Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[24]  E. Niebur,et al.  Growth patterns in the developing brain detected by using continuum mechanical tensor maps , 2022 .

[25]  Arup Roy,et al.  Rate Limitations of Unitary Event Analysis , 2000, Neural Computation.

[26]  L. Paninski,et al.  Information about movement direction obtained from synchronous activity of motor cortical neurons. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[27]  W. Newsome,et al.  The Variable Discharge of Cortical Neurons: Implications for Connectivity, Computation, and Information Coding , 1998, The Journal of Neuroscience.

[28]  Frank Rosenblatt,et al.  PRINCIPLES OF NEURODYNAMICS. PERCEPTRONS AND THE THEORY OF BRAIN MECHANISMS , 1963 .

[29]  Wolf Singer,et al.  Striving for coherence , 1999 .

[30]  W. Singer,et al.  Neuronal assemblies: necessity, signature and detectability , 1997, Trends in Cognitive Sciences.

[31]  K. Martin The Pope and grandmother–a frog's-eye view of theory , 2000, Nature Neuroscience.

[32]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[33]  Sonja Grün,et al.  Dynamical changes and temporal precision of synchronized spiking activity in monkey motor cortex during movement preparation , 2000, Journal of Physiology-Paris.

[34]  J J Eggermont,et al.  Neural interaction in cat primary auditory cortex II. Effects of sound stimulation. , 1994, Journal of neurophysiology.

[35]  E Ahissar,et al.  Neural interactions in the frontal cortex of a behaving monkey: signs of dependence on stimulus context and behavioral state. , 1991, Journal fur Hirnforschung.

[36]  A Bastian,et al.  Prior information preshapes the population representation of movement direction in motor cortex , 1998, Neuroreport.

[37]  Wolf Singer,et al.  Neuronal Synchrony: A Versatile Code for the Definition of Relations? , 1999, Neuron.

[38]  Sonja Grün,et al.  Unitary Events in Multiple Single-Neuron Spiking Activity: II. Nonstationary Data , 2002, Neural Computation.

[39]  H B Barlow,et al.  Single units and sensation: a neuron doctrine for perceptual psychology? , 1972, Perception.

[40]  C. V. D. Malsburg,et al.  Frank Rosenblatt: Principles of Neurodynamics: Perceptrons and the Theory of Brain Mechanisms , 1986 .

[41]  W. Singer,et al.  Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[42]  W. Pitts,et al.  A Logical Calculus of the Ideas Immanent in Nervous Activity (1943) , 2021, Ideas That Created the Future.

[43]  DiesmannMarkus,et al.  Unitary events in multiple single-neuron spiking activity , 2002 .

[44]  E. Vaadia,et al.  Spatiotemporal firing patterns in the frontal cortex of behaving monkeys. , 1993, Journal of neurophysiology.

[45]  Prof. Dr. Valentino Braitenberg,et al.  Anatomy of the Cortex , 1991, Studies of Brain Function.

[46]  J. Bullier,et al.  Structural basis of cortical synchronization. I. Three types of interhemispheric coupling. , 1995, Journal of neurophysiology.

[47]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

[48]  W. Singer,et al.  Temporal coding in the visual cortex: new vistas on integration in the nervous system , 1992, Trends in Neurosciences.

[49]  Pablo Fuentealba,et al.  Synaptic interactions between thalamic and cortical inputs onto cortical neurons in vivo. , 2004, Journal of neurophysiology.

[50]  Ad Aertsen,et al.  Stable propagation of synchronous spiking in cortical neural networks , 1999, Nature.

[51]  E. Ahissar,et al.  Correlated Activity of Neurons: A Neural Code for Higher Brain Functions? , 1991 .

[52]  Janak H. Patel,et al.  Model of Computation , 1990 .

[53]  M. Nicolelis,et al.  Sensorimotor encoding by synchronous neural ensemble activity at multiple levels of the somatosensory system. , 1995, Science.

[54]  W. Pitts,et al.  What the Frog's Eye Tells the Frog's Brain , 1959, Proceedings of the IRE.

[55]  John J. Hopfield,et al.  Neural networks and physical systems with emergent collective computational abilities , 1999 .

[56]  W. Singer,et al.  The Role of Neuronal Synchronization in Response Selection: A Biologically Plausible Theory of Structured Representations in the Visual Cortex , 1996, Journal of Cognitive Neuroscience.

[57]  M. Ahissar,et al.  Encoding of sound-source location and movement: activity of single neurons and interactions between adjacent neurons in the monkey auditory cortex. , 1992, Journal of neurophysiology.

[58]  Sonja Grün,et al.  Unitary joint events in multiple neuron spiking activity: detection, significance, and interpretation , 1996 .

[59]  A. Aertsen,et al.  Neuronal assemblies , 1989, IEEE Transactions on Biomedical Engineering.

[60]  Daniel J. Amit,et al.  Modeling brain function: the world of attractor neural networks, 1st Edition , 1989 .

[61]  Christoph von der Malsburg,et al.  The Correlation Theory of Brain Function , 1994 .

[62]  D. Georgescauld Local Cortical Circuits, An Electrophysiological Study , 1983 .

[63]  M K Habib,et al.  Dynamics of neuronal firing correlation: modulation of "effective connectivity". , 1989, Journal of neurophysiology.

[64]  Stuart N. Baker,et al.  An Accurate Measure of the Instantaneous Discharge Probability, with Application to Unitary Joint-Event Analysis , 2000, Neural Computation.

[65]  H. L. Bryant,et al.  Spike initiation by transmembrane current: a white‐noise analysis. , 1976, The Journal of physiology.

[66]  Valentino Braitenberg,et al.  Information Processing in the Cortex , 1992, Springer Berlin Heidelberg.

[67]  R. Eckhorn,et al.  Coherent oscillations: A mechanism of feature linking in the visual cortex? , 1988, Biological Cybernetics.

[68]  Sonja Grün,et al.  Detecting unitary events without discretization of time , 1999, Journal of Neuroscience Methods.

[69]  Moshe Abeles,et al.  Corticonics: Neural Circuits of Cerebral Cortex , 1991 .

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

[71]  M. Abeles Role of the cortical neuron: integrator or coincidence detector? , 1982, Israel journal of medical sciences.

[72]  D. H. Paul The physiology of nerve cells , 1975 .

[73]  E. D. Adrian,et al.  The Basis of Sensation , 1928, The Indian Medical Gazette.

[74]  J. T. Massey,et al.  Mental rotation of the neuronal population vector. , 1989, Science.

[75]  W. Singer Synchronization of cortical activity and its putative role in information processing and learning. , 1993, Annual review of physiology.

[76]  M. Abeles Local Cortical Circuits: An Electrophysiological Study , 1982 .

[77]  R. Christopher deCharms,et al.  Primary cortical representation of sounds by the coordination of action-potential timing , 1996, Nature.

[78]  D. Amit,et al.  Model of global spontaneous activity and local structured activity during delay periods in the cerebral cortex. , 1997, Cerebral cortex.

[79]  M. Abeles,et al.  Neuronal activities related to higher brain functions-theoretical and experimental implications , 1989, IEEE Transactions on Biomedical Engineering.

[80]  Yoshio Sakurai,et al.  Population coding by cell assemblies—what it really is in the brain , 1996, Neuroscience Research.

[81]  E. Vaadia,et al.  Spatiotemporal structure of cortical activity: properties and behavioral relevance. , 1998, Journal of neurophysiology.

[82]  C. von der Malsburg,et al.  Am I Thinking Assemblies , 1986 .

[83]  Marc-Oliver Gewaltig,et al.  A model of computation in neocortical architecture , 1999, Neural Networks.

[84]  A. P. Georgopoulos,et al.  Primate motor cortex and free arm movements to visual targets in three- dimensional space. II. Coding of the direction of movement by a neuronal population , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[85]  Jamie Goode,et al.  Complexity in Biological Information Processing , 2001 .