Literature DB >> 27511007

Synchronous Spike Patterns in Macaque Motor Cortex during an Instructed-Delay Reach-to-Grasp Task.

Emiliano Torre1, Pietro Quaglio1, Michael Denker1, Thomas Brochier2, Alexa Riehle3, Sonja Grün4.   

Abstract

UNLABELLED: The computational role of spike time synchronization at millisecond precision among neurons in the cerebral cortex is hotly debated. Studies performed on data of limited size provided experimental evidence that low-order correlations occur in relation to behavior. Advances in electrophysiological technology to record from hundreds of neurons simultaneously provide the opportunity to observe coordinated spiking activity of larger populations of cells. We recently published a method that combines data mining and statistical evaluation to search for significant patterns of synchronous spikes in massively parallel spike trains (Torre et al., 2013). The method solves the computational and multiple testing problems raised by the high dimensionality of the data. In the current study, we used our method on simultaneous recordings from two macaque monkeys engaged in an instructed-delay reach-to-grasp task to determine the emergence of spike synchronization in relation to behavior. We found a multitude of synchronous spike patterns aligned in both monkeys along a preferential mediolateral orientation in brain space. The occurrence of the patterns is highly specific to behavior, indicating that different behaviors are associated with the synchronization of different groups of neurons ("cell assemblies"). However, pooled patterns that overlap in neuronal composition exhibit no specificity, suggesting that exclusive cell assemblies become active during different behaviors, but can recruit partly identical neurons. These findings are consistent across multiple recording sessions analyzed across the two monkeys. SIGNIFICANCE STATEMENT: Neurons in the brain communicate via electrical impulses called spikes. How spikes are coordinated to process information is still largely unknown. Synchronous spikes are effective in triggering a spike emission in receiving neurons and have been shown to occur in relation to behavior in a number of studies on simultaneous recordings of few neurons. We recently published a method to extend this type of investigation to larger data. Here, we apply it to simultaneous recordings of hundreds of neurons from the motor cortex of macaque monkeys performing a motor task. Our analysis reveals groups of neurons selectively synchronizing their activity in relation to behavior, which sheds new light on the role of synchrony in information processing in the cerebral cortex.
Copyright © 2016 Torre, et al.

Keywords:  cell assemblies; massively parallel spike trains; motor cortex; spike synchrony; temporal coding

Mesh:

Year:  2016        PMID: 27511007      PMCID: PMC4978798          DOI: 10.1523/JNEUROSCI.4375-15.2016

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  36 in total

1.  Stable propagation of synchronous spiking in cortical neural networks.

Authors:  M Diesmann; M O Gewaltig; A Aertsen
Journal:  Nature       Date:  1999-12-02       Impact factor: 49.962

2.  Polychronization: computation with spikes.

Authors:  Eugene M Izhikevich
Journal:  Neural Comput       Date:  2006-02       Impact factor: 2.026

3.  Propagating waves mediate information transfer in the motor cortex.

Authors:  Doug Rubino; Kay A Robbins; Nicholas G Hatsopoulos
Journal:  Nat Neurosci       Date:  2006-11-19       Impact factor: 24.884

4.  Synaptic interactions between forelimb-related motor cortex neurons in behaving primates.

Authors:  W S Smith; E E Fetz
Journal:  J Neurophysiol       Date:  2009-05-13       Impact factor: 2.714

5.  Dynamics of neuronal interactions in monkey cortex in relation to behavioural events.

Authors:  E Vaadia; I Haalman; M Abeles; H Bergman; Y Prut; H Slovin; A Aertsen
Journal:  Nature       Date:  1995-02-09       Impact factor: 49.962

6.  Role of the cortical neuron: integrator or coincidence detector?

Authors:  M Abeles
Journal:  Isr J Med Sci       Date:  1982-01

7.  Synchronization of neurons during local field potential oscillations in sensorimotor cortex of awake monkeys.

Authors:  V N Murthy; E E Fetz
Journal:  J Neurophysiol       Date:  1996-12       Impact factor: 2.714

8.  Motor aspects of cue-related neuronal activity in premotor cortex of the rhesus monkey.

Authors:  S P Wise; M Weinrich; K H Mauritz
Journal:  Brain Res       Date:  1983-02-07       Impact factor: 3.252

9.  Mapping the spatio-temporal structure of motor cortical LFP and spiking activities during reach-to-grasp movements.

Authors:  Alexa Riehle; Sarah Wirtssohn; Sonja Grün; Thomas Brochier
Journal:  Front Neural Circuits       Date:  2013-03-27       Impact factor: 3.492

10.  Large-scale spatiotemporal spike patterning consistent with wave propagation in motor cortex.

Authors:  Kazutaka Takahashi; Sanggyun Kim; Todd P Coleman; Kevin A Brown; Aaron J Suminski; Matthew D Best; Nicholas G Hatsopoulos
Journal:  Nat Commun       Date:  2015-05-21       Impact factor: 14.919

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  14 in total

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Authors:  Jingwen Li; Patrick A Kells; Ayla C Osgood; Shree Hari Gautam; Woodrow L Shew
Journal:  Proc Natl Acad Sci U S A       Date:  2021-10-26       Impact factor: 11.205

2.  On the Complexity of Resting State Spiking Activity in Monkey Motor Cortex.

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3.  Global organization of neuronal activity only requires unstructured local connectivity.

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4.  Serial Spike Time Correlations Affect Probability Distribution of Joint Spike Events.

Authors:  Mina Shahi; Carl van Vreeswijk; Gordon Pipa
Journal:  Front Comput Neurosci       Date:  2016-12-23       Impact factor: 2.380

5.  PRANAS: A New Platform for Retinal Analysis and Simulation.

Authors:  Bruno Cessac; Pierre Kornprobst; Selim Kraria; Hassan Nasser; Daniela Pamplona; Geoffrey Portelli; Thierry Viéville
Journal:  Front Neuroinform       Date:  2017-09-01       Impact factor: 4.081

6.  Detection and Evaluation of Spatio-Temporal Spike Patterns in Massively Parallel Spike Train Data with SPADE.

Authors:  Pietro Quaglio; Alper Yegenoglu; Emiliano Torre; Dominik M Endres; Sonja Grün
Journal:  Front Comput Neurosci       Date:  2017-05-24       Impact factor: 2.380

7.  Cell assemblies at multiple time scales with arbitrary lag constellations.

Authors:  Eleonora Russo; Daniel Durstewitz
Journal:  Elife       Date:  2017-01-11       Impact factor: 8.140

8.  Methods for identification of spike patterns in massively parallel spike trains.

Authors:  Pietro Quaglio; Vahid Rostami; Emiliano Torre; Sonja Grün
Journal:  Biol Cybern       Date:  2018-04-12       Impact factor: 2.086

9.  LFP beta amplitude is linked to mesoscopic spatio-temporal phase patterns.

Authors:  Michael Denker; Lyuba Zehl; Bjørg E Kilavik; Markus Diesmann; Thomas Brochier; Alexa Riehle; Sonja Grün
Journal:  Sci Rep       Date:  2018-03-26       Impact factor: 4.379

10.  Massively parallel recordings in macaque motor cortex during an instructed delayed reach-to-grasp task.

Authors:  Thomas Brochier; Lyuba Zehl; Yaoyao Hao; Margaux Duret; Julia Sprenger; Michael Denker; Sonja Grün; Alexa Riehle
Journal:  Sci Data       Date:  2018-04-10       Impact factor: 6.444

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