Literature DB >> 29798892

Neural Dynamics of Variable Grasp-Movement Preparation in the Macaque Frontoparietal Network.

Jonathan A Michaels1,2,3, Benjamin Dann1, Rijk W Intveld1, Hansjörg Scherberger4,5.   

Abstract

Our voluntary grasping actions lie on a continuum between immediate action and waiting for the right moment, depending on the context. Therefore, studying grasping requires an investigation into how preparation time affects this process. Two macaque monkeys (Macaca mulatta; one male, one female) performed a grasping task with a short instruction followed by an immediate or delayed go cue (0-1300 ms) while we recorded in parallel from neurons in the grasp preparation relevant area F5 that is part of the ventral premotor cortex, and the anterior intraparietal area (AIP). Initial population dynamics followed a fixed trajectory in the neural state space unique to each grip type, reflecting unavoidable movement selection, then diverged depending on the delay, reaching unique states not achieved for immediately cued movements. Population activity in the AIP was less dynamic, whereas F5 activity continued to evolve throughout the delay. Interestingly, neuronal populations from both areas allowed for a readout tracking subjective anticipation of the go cue that predicted single-trial reaction time. However, the prediction of reaction time was better from F5 activity. Intriguingly, activity during movement initiation clustered into two trajectory groups, corresponding to movements that were either "as fast as possible" or withheld movements, demonstrating a widespread state shift in the frontoparietal grasping network when movements must be withheld. Our results reveal how dissociation between immediate and delay-specific preparatory activity, as well as differentiation between cortical areas, is possible through population-level analysis.SIGNIFICANCE STATEMENT Sometimes when we move, we consciously plan our movements. At other times, we move instantly, seemingly with no planning at all. Yet, it's unclear how preparation for movements along this spectrum of planned and seemingly unplanned movement differs in the brain. Two macaque monkeys made reach-to-grasp movements after varying amounts of preparation time while we recorded from the premotor and parietal cortex. We found that the initial response to a grasp instruction was specific to the required movement, but not to the preparation time, reflecting required movement selection. However, when more preparation time was given, neural activity achieved unique states that likely related to withholding movements and anticipation of movement, shedding light on the roles of the premotor and parietal cortex in grasp planning.
Copyright © 2018 the authors 0270-6474/18/385759-15$15.00/0.

Entities:  

Keywords:  grasping; motor; parietal; population analysis; premotor; primate

Mesh:

Year:  2018        PMID: 29798892      PMCID: PMC6595979          DOI: 10.1523/JNEUROSCI.2557-17.2018

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


  53 in total

1.  Representation of time by neurons in the posterior parietal cortex of the macaque.

Authors:  Matthew I Leon; Michael N Shadlen
Journal:  Neuron       Date:  2003-04-24       Impact factor: 17.173

2.  Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering.

Authors:  R Quian Quiroga; Z Nadasdy; Y Ben-Shaul
Journal:  Neural Comput       Date:  2004-08       Impact factor: 2.026

3.  Context-specific grasp movement representation in macaque ventral premotor cortex.

Authors:  Marie-Christine Fluet; Markus A Baumann; Hansjörg Scherberger
Journal:  J Neurosci       Date:  2010-11-10       Impact factor: 6.167

4.  Preparatory delay activity in the monkey parietal reach region predicts reach reaction times.

Authors:  Lawrence H Snyder; Anthony R Dickinson; Jeffrey L Calton
Journal:  J Neurosci       Date:  2006-10-04       Impact factor: 6.167

5.  Gaussian-process factor analysis for low-dimensional single-trial analysis of neural population activity.

Authors:  Byron M Yu; John P Cunningham; Gopal Santhanam; Stephen I Ryu; Krishna V Shenoy; Maneesh Sahani
Journal:  J Neurophysiol       Date:  2009-04-08       Impact factor: 2.714

6.  Delay in the execution of voluntary movement by electrical or magnetic brain stimulation in intact man. Evidence for the storage of motor programs in the brain.

Authors:  B L Day; J C Rothwell; P D Thompson; A Maertens de Noordhout; K Nakashima; K Shannon; C D Marsden
Journal:  Brain       Date:  1989-06       Impact factor: 13.501

7.  Corticocortical connections of area F3 (SMA-proper) and area F6 (pre-SMA) in the macaque monkey.

Authors:  G Luppino; M Matelli; R Camarda; G Rizzolatti
Journal:  J Comp Neurol       Date:  1993-12-01       Impact factor: 3.215

8.  The Largest Response Component in the Motor Cortex Reflects Movement Timing but Not Movement Type.

Authors:  Matthew T Kaufman; Jeffrey S Seely; David Sussillo; Stephen I Ryu; Krishna V Shenoy; Mark M Churchland
Journal:  eNeuro       Date:  2016-08-30

9.  Neural Population Dynamics during Reaching Are Better Explained by a Dynamical System than Representational Tuning.

Authors:  Jonathan A Michaels; Benjamin Dann; Hansjörg Scherberger
Journal:  PLoS Comput Biol       Date:  2016-11-04       Impact factor: 4.475

10.  Population coding of grasp and laterality-related information in the macaque fronto-parietal network.

Authors:  Jonathan A Michaels; Hansjörg Scherberger
Journal:  Sci Rep       Date:  2018-01-26       Impact factor: 4.379

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  8 in total

Review 1.  Latent Factors and Dynamics in Motor Cortex and Their Application to Brain-Machine Interfaces.

Authors:  Chethan Pandarinath; K Cora Ames; Abigail A Russo; Ali Farshchian; Lee E Miller; Eva L Dyer; Jonathan C Kao
Journal:  J Neurosci       Date:  2018-10-31       Impact factor: 6.167

2.  Conservation of preparatory neural events in monkey motor cortex regardless of how movement is initiated.

Authors:  Antonio H Lara; Gamaleldin F Elsayed; Andrew J Zimnik; John P Cunningham; Mark M Churchland
Journal:  Elife       Date:  2018-08-22       Impact factor: 8.140

3.  Movement initiation and grasp representation in premotor and primary motor cortex mirror neurons.

Authors:  Steven Jack Jerjian; Maneesh Sahani; Alexander Kraskov
Journal:  Elife       Date:  2020-07-06       Impact factor: 8.140

4.  Repetita iuvant: repetition facilitates online planning of sequential movements.

Authors:  Giacomo Ariani; Young Han Kwon; Jörn Diedrichsen
Journal:  J Neurophysiol       Date:  2020-03-25       Impact factor: 2.714

5.  Cortical population activity within a preserved neural manifold underlies multiple motor behaviors.

Authors:  Juan A Gallego; Matthew G Perich; Stephanie N Naufel; Christian Ethier; Sara A Solla; Lee E Miller
Journal:  Nat Commun       Date:  2018-10-12       Impact factor: 14.919

6.  Neural coding of intended and executed grasp force in macaque areas AIP, F5, and M1.

Authors:  Rijk W Intveld; Benjamin Dann; Jonathan A Michaels; Hansjörg Scherberger
Journal:  Sci Rep       Date:  2018-12-20       Impact factor: 4.379

Review 7.  Emerging ideas and tools to study the emergent properties of the cortical neural circuits for voluntary motor control in non-human primates.

Authors:  John F Kalaska
Journal:  F1000Res       Date:  2019-05-29

8.  Neural population dynamics in motor cortex are different for reach and grasp.

Authors:  Aneesha K Suresh; James M Goodman; Elizaveta V Okorokova; Matthew Kaufman; Nicholas G Hatsopoulos; Sliman J Bensmaia
Journal:  Elife       Date:  2020-11-17       Impact factor: 8.140

  8 in total

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