Reliable Sequential Activation of Neural Assemblies by Single Pyramidal Cells in a Three-Layered Cortex

Recent studies reveal the occasional impact of single neurons on surround firing statistics and even simple behaviors. Exploiting the advantages of a simple cortex, we examined the influence of single pyramidal neurons on surrounding cortical circuits. Brief activation of single neurons triggered reliable sequences of firing in tens of other excitatory and inhibitory cortical neurons, reflecting cascading activity through local networks, as indicated by delayed yet precisely timed polysynaptic subthreshold potentials. The evoked patterns were specific to the pyramidal cell of origin, extended over hundreds of micrometers from their source, and unfolded over up to 200 ms. Simultaneous activation of pyramidal cell pairs indicated balanced control of population activity, preventing paroxysmal amplification. Single cortical pyramidal neurons can thus trigger reliable postsynaptic activity that can propagate in a reliable fashion through cortex, generating rapidly evolving and non-random firing sequences reminiscent of those observed in mammalian hippocampus during "replay" and in avian song circuits.

[1]  H. Sompolinsky,et al.  Chaos in Neuronal Networks with Balanced Excitatory and Inhibitory Activity , 1996, Science.

[2]  Karl J. Friston.  The free-energy principle: a unified brain theory? , 2010, Nature Reviews Neuroscience.

[3]  P. Somogyi,et al.  Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo , 2003, Nature.

[4]  G. Dragoi,et al.  Preplay of future place cell sequences by hippocampal cellular assemblies , 2011, Nature.

[5]  Y. Dan,et al.  Burst Spiking of a Single Cortical Neuron Modifies Global Brain State , 2009, Science.

[6]  J. Griffith.  On the stability of brain-like structures. , 1963, Biophysical journal.

[7]  Jean-Pierre Eckmann,et al.  Leader neurons in population bursts of 2D living neural networks , 2008 .

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

[9]  Tracy M. Yamawaki,et al.  Evolution of pallium, hippocampus, and cortical cell types revealed by single-cell transcriptomics in reptiles , 2018, Science.

[10]  Lorenz Pammer,et al.  Comparative approaches to cortical microcircuits , 2016, Current Opinion in Neurobiology.

[11]  George Dragoi,et al.  Distinct preplay of multiple novel spatial experiences in the rat , 2013, Proceedings of the National Academy of Sciences.

[12]  B W Connors,et al.  Cellular physiology of the turtle visual cortex: synaptic properties and intrinsic circuitry , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  M. Fee,et al.  Using temperature to analyze temporal dynamics in the songbird motor pathway , 2008, Nature.

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

[15]  R. Yuste,et al.  Optical probing of neuronal circuits with calcium indicators. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Rainer W. Friedrich,et al.  Olfactory pattern classification by discrete neuronal network states , 2010, Nature.

[17]  Michael J. Berry,et al.  Weak pairwise correlations imply strongly correlated network states in a neural population , 2005, Nature.

[18]  Gilles Laurent,et al.  Transient Dynamics for Neural Processing , 2008, Science.

[19]  Z. Molnár,et al.  From sauropsids to mammals and back: New approaches to comparative cortical development , 2015, The Journal of comparative neurology.

[20]  L. Puelles,et al.  1.26 – The Pallium in Reptiles and Birds in the Light of the Updated Tetrapartite Pallium Model , 2017 .

[21]  J. Fournier,et al.  Spatial Information in a Non-retinotopic Visual Cortex , 2018, Neuron.

[22]  Karl Deisseroth,et al.  Optogenetics in Neural Systems , 2011, Neuron.

[23]  K. Harris,et al.  Spontaneous Events Outline the Realm of Possible Sensory Responses in Neocortical Populations , 2009, Neuron.

[24]  G. Buzsáki,et al.  Sequential structure of neocortical spontaneous activity in vivo , 2007, Proceedings of the National Academy of Sciences.

[25]  M. London,et al.  Sensitivity to perturbations in vivo implies high noise and suggests rate coding in cortex , 2010, Nature.

[26]  Rune W. Berg,et al.  Balanced Inhibition and Excitation Drive Spike Activity in Spinal Half-Centers , 2007, Science.

[27]  G. Buzsáki,et al.  Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo , 2002, Nature Neuroscience.

[28]  Eugene M. Izhikevich,et al.  Polychronization: Computation with Spikes , 2006, Neural Computation.

[29]  Peter Rupprecht,et al.  Precise Synaptic Balance in the Zebrafish Homolog of Olfactory Cortex , 2018, Neuron.

[30]  Woodrow L. Shew,et al.  Adaptation to sensory input tunes visual cortex to criticality , 2015, Nature Physics.

[31]  M. Scanziani,et al.  How Inhibition Shapes Cortical Activity , 2011, Neuron.

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

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

[34]  Lorenz Pammer,et al.  Large-scale mapping of cortical synaptic projections with extracellular electrode arrays , 2017, Nature Methods.

[35]  R. Miles,et al.  Single CA3 pyramidal cells trigger sharp waves in vitro by exciting interneurones , 2016, The Journal of physiology.

[36]  Benjamin A. Dunn,et al.  Recurrent inhibitory circuitry as a mechanism for grid formation , 2013, Nature Neuroscience.

[37]  Peter Jonas,et al.  Plasticity-dependent, full detonation at hippocampal mossy fiber–CA3 pyramidal neuron synapses , 2016, eLife.

[38]  Richard Hans Robert Hahnloser,et al.  An ultra-sparse code underliesthe generation of neural sequences in a songbird , 2002, Nature.

[39]  Kevin L. Briggman,et al.  Optical Imaging of Neuronal Populations During Decision-Making , 2005, Science.

[40]  Csaba Varga,et al.  Complex Events Initiated by Individual Spikes in the Human Cerebral Cortex , 2008, PLoS biology.

[41]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[42]  Tatsuo S. Okubo,et al.  Growth and splitting of neural sequences in songbird vocal development , 2015, Nature.

[43]  W. James,et al.  The Principles of Psychology. , 1983 .

[44]  L. Abbott,et al.  Neural network dynamics. , 2005, Annual review of neuroscience.

[45]  P. Z. Mazurskaya.  Organization of receptive fields in the forebrain ofEmys orbicularis , 1973, Neuroscience and Behavioral Physiology.

[46]  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.

[47]  P. Z. Mazurskaya.  Retinal projection in the forebrain ofEmys orbicularis , 2005, Neuroscience and Behavioral Physiology.

[48]  J. Csicsvari,et al.  Replay and Time Compression of Recurring Spike Sequences in the Hippocampus , 1999, The Journal of Neuroscience.

[49]  G. Striedter.  The telencephalon of tetrapods in evolution. , 1997, Brain, behavior and evolution.

[50]  Lilach Avitan,et al.  Emergence of spontaneous assembly activity in developing neural networks without afferent input , 2018, PLoS Comput. Biol..

[51]  G. Laurent,et al.  Dynamic optimization of odor representations by slow temporal patterning of mitral cell activity. , 2001, Science.

[52]  F. Attneave,et al.  The Organization of Behavior: A Neuropsychological Theory , 1949 .

[53]  Karl J. Friston,et al.  Does predictive coding have a future? , 2018, Nature Neuroscience.

[54]  Pablo Varona,et al.  Robust Transient Dynamics and Brain Functions , 2011, Front. Comput. Neurosci..

[55]  Tracy M. Yamawaki,et al.  The reptilian brain , 2015, Current Biology.

[56]  Gilles Laurent,et al.  Olfactory network dynamics and the coding of multidimensional signals , 2002, Nature Reviews Neuroscience.

[57]  David J. Foster,et al.  Reverse replay of behavioural sequences in hippocampal place cells during the awake state , 2006, Nature.

[58]  Simon X. Chen,et al.  Emergence of reproducible spatiotemporal activity during motor learning , 2014, Nature.

[59]  B. McNaughton,et al.  Packet-based communication in the cortex , 2015, Nature Reviews Neuroscience.

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

[61]  E. P. Gardner,et al.  Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex , 2008, Nature Reviews Neuroscience.

[62]  Luca Berdondini,et al.  Recurrently connected and localized neuronal communities initiate coordinated spontaneous activity in neuronal networks , 2017, PLoS Comput. Biol..

[63]  C. Petersen,et al.  The Excitatory Neuronal Network of the C2 Barrel Column in Mouse Primary Somatosensory Cortex , 2009, Neuron.

[64]  G. Laurent,et al.  Transient Dynamics versus Fixed Points in Odor Representations by Locust Antennal Lobe Projection Neurons , 2005, Neuron.

[65]  Sen Song,et al.  Highly Nonrandom Features of Synaptic Connectivity in Local Cortical Circuits , 2005, PLoS biology.

[66]  A. Aertsen,et al.  Spiking activity propagation in neuronal networks: reconciling different perspectives on neural coding , 2010, Nature Reviews Neuroscience.

[67]  B J Richmond,et al.  Stochastic nature of precisely timed spike patterns in visual system neuronal responses. , 1999, Journal of neurophysiology.

[68]  Richard Hans Robert Hahnloser,et al.  Spike-Time-Dependent Plasticity and Heterosynaptic Competition Organize Networks to Produce Long Scale-Free Sequences of Neural Activity , 2010, Neuron.

[69]  V. Jayaraman,et al.  Intensity versus Identity Coding in an Olfactory System , 2003, Neuron.

[70]  Matthew T. Kaufman,et al.  Neural population dynamics during reaching , 2012, Nature.

[71]  B. Sakmann,et al.  Whisker movements evoked by stimulation of single pyramidal cells in rat motor cortex , 2004, Nature.

[72]  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.

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

[74]  E. Bienenstock.  A model of neocortex , 1995 .

[75]  G. Laurent,et al.  Odor encoding as an active, dynamical process: experiments, computation, and theory. , 2001, Annual review of neuroscience.

[76]  Michel A. Picardo,et al.  GABAergic Hub Neurons Orchestrate Synchrony in Developing Hippocampal Networks , 2009, Science.

[77]  Eero P. Simoncelli,et al.  Spatio-temporal correlations and visual signalling in a complete neuronal population , 2008, Nature.

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

[79]  M. Brecht,et al.  Behavioural report of single neuron stimulation in somatosensory cortex , 2008, Nature.

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

[81]  A. Reyes.  Synchrony-dependent propagation of firing rate in iteratively constructed networks in vitro , 2003, Nature Neuroscience.

[82]  G. Buzsáki,et al.  Forward and reverse hippocampal place-cell sequences during ripples , 2007, Nature Neuroscience.

[83]  G. Laurent,et al.  Multiplexing using synchrony in the zebrafish olfactory bulb , 2004, Nature Neuroscience.

[84]  Gerald E. Hough,et al.  Avian brains and a new understanding of vertebrate brain evolution , 2005, Nature Reviews Neuroscience.

[85]  J. Fournier,et al.  Looking for the roots of cortical sensory computation in three-layered cortices , 2015, Current Opinion in Neurobiology.

[86]  Dezhe Z. Jin,et al.  Support for a synaptic chain model of neuronal sequence generation , 2010, Nature.

[87]  Alexander Borst,et al.  The TREES Toolbox—Probing the Basis of Axonal and Dendritic Branching , 2011, Neuroinformatics.

[88]  B W Connors,et al.  Cellular physiology of the turtle visual cortex: distinctive properties of pyramidal and stellate neurons , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.