What is a moment? Transient synchrony as a collective mechanism for spatiotemporal integration.

A previous paper described a network of simple integrate-and-fire neurons that contained output neurons selective for specific spatiotemporal patterns of inputs; only experimental results were described. We now present the principles behind the operation of this network and discuss how these principles point to a general class of computational operations that can be carried out easily and naturally by networks of spiking neurons. Transient synchrony of the action potentials of a group of neurons is used to signal "recognition" of a space-time pattern across the inputs of those neurons. Appropriate synaptic coupling produces synchrony when the inputs to these neurons are nearly equal, leaving the neurons unsynchronized or only weakly synchronized for other input circumstances. When the input to this system comes from timed past events represented by decaying delay activity, the pattern of synaptic connections can be set such that synchronization occurs only for selected spatiotemporal patterns. We show how the recognition is invariant to uniform time warp and uniform intensity change of the input events. The fundamental recognition event is a transient collective synchronization, representing "many neurons now agree," an event that is then detected easily by a cell with a small time constant. If such synchronization is used in neurobiological computation, its hallmark will be a brief burst of gamma-band electroencephalogram noise when and where such a recognition event or decision occurs.

[1]  E. Adrian.  Olfactory reactions in the brain of the hedgehog , 1942, The Journal of physiology.

[2]  B. Mandelbrot,et al.  RANDOM WALK MODELS FOR THE SPIKE ACTIVITY OF A SINGLE NEURON. , 1964, Biophysical journal.

[3]  J. Nicholls.  From neuron to brain , 1976 .

[4]  R. A. Davidoff.  From Neuron to Brain , 1977, Neurology.

[5]  H Sompolinsky,et al.  Global processing of visual stimuli in a neural network of coupled oscillators. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[6]  S. Strogatz,et al.  Dynamics of a large system of coupled nonlinear oscillators , 1991 .

[7]  Sompolinsky,et al.  Pattern of synchrony in inhomogeneous networks of oscillators with pulse interactions. , 1993, Physical review letters.

[8]  D. Tank,et al.  In Vivo Ca2+ Dynamics in a Cricket Auditory Neuron: An Example of Chemical Computation , 1994, Science.

[9]  Michael N. Shadlen,et al.  Noise, neural codes and cortical organization , 1994, Current Opinion in Neurobiology.

[10]  M M Merzenich,et al.  Temporal information transformed into a spatial code by a neural network with realistic properties , 1995, Science.

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

[12]  Jane S. Paulsen.  Memory in the Cerebral Cortex: An Empirical Approach to Neural Networks in the Human and Nonhuman Primate , 1996 .

[13]  G. Laurent,et al.  Odour encoding by temporal sequences of firing in oscillating neural assemblies , 1996, Nature.

[14]  J J Hopfield,et al.  Transforming neural computations and representing time. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[15]  H. Markram,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997, Science.

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

[17]  Carlos D. Brody,et al.  Computing with Action Potentials , 1997, NIPS.

[18]  Haim Sompolinsky,et al.  Chaotic Balanced State in a Model of Cortical Circuits , 1998, Neural Computation.

[19]  P. Goldman-Rakic,et al.  Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working memory task. , 1998, Journal of neurophysiology.

[20]  G. Bi,et al.  Synaptic Modifications in Cultured Hippocampal Neurons: Dependence on Spike Timing, Synaptic Strength, and Postsynaptic Cell Type , 1998, The Journal of Neuroscience.

[21]  Matthias M. Müller,et al.  Human Gamma Band Activity and Perception of a Gestalt , 1999, The Journal of Neuroscience.

[22]  R. Romo,et al.  Neuronal correlates of parametric working memory in the prefrontal cortex , 1999, Nature.

[23]  J J Hopfield,et al.  Odor space and olfactory processing: collective algorithms and neural implementation. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[24]  B. Connors,et al.  Two networks of electrically coupled inhibitory neurons in neocortex , 1999, Nature.

[25]  The Sign of the Four , 1999 .

[26]  J J Hopfield,et al.  What is a moment? "Cortical" sensory integration over a brief interval. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[27]  R. Romo,et al.  Periodicity and Firing Rate As Candidate Neural Codes for the Frequency of Vibrotactile Stimuli , 2000, The Journal of Neuroscience.