Literature DB >> 29357477

Emergent coordination underlying learning to reach to grasp with a brain-machine interface.

Mukta Vaidya1,2, Karthikeyan Balasubramanian3, Joshua Southerland4, Islam Badreldin5, Ahmed Eleryan6, Kelsey Shattuck7, Suchin Gururangan1, Marc Slutzky2, Leslie Osborne8, Andrew Fagg4, Karim Oweiss5,9,10, Nicholas G Hatsopoulos1,3.   

Abstract

The development of coordinated reach-to-grasp movement has been well studied in infants and children. However, the role of motor cortex during this development is unclear because it is difficult to study in humans. We took the approach of using a brain-machine interface (BMI) paradigm in rhesus macaques with prior therapeutic amputations to examine the emergence of novel, coordinated reach to grasp. Previous research has shown that after amputation, the cortical area previously involved in the control of the lost limb undergoes reorganization, but prior BMI work has largely relied on finding neurons that already encode specific movement-related information. In this study, we taught macaques to cortically control a robotic arm and hand through operant conditioning, using neurons that were not explicitly reach or grasp related. Over the course of training, stereotypical patterns emerged and stabilized in the cross-covariance between the reaching and grasping velocity profiles, between pairs of neurons involved in controlling reach and grasp, and to a comparable, but lesser, extent between other stable neurons in the network. In fact, we found evidence of this structured coordination between pairs composed of all combinations of neurons decoding reach or grasp and other stable neurons in the network. The degree of and participation in coordination was highly correlated across all pair types. Our approach provides a unique model for studying the development of novel, coordinated reach-to-grasp movement at the behavioral and cortical levels. NEW & NOTEWORTHY Given that motor cortex undergoes reorganization after amputation, our work focuses on training nonhuman primates with chronic amputations to use neurons that are not reach or grasp related to control a robotic arm to reach to grasp through the use of operant conditioning, mimicking early development. We studied the development of a novel, coordinated behavior at the behavioral and cortical level, and the neural plasticity in M1 associated with learning to use a brain-machine interface.

Entities:  

Keywords:  brain-machine interfaces; learning; neural coordination; primary motor cortex; reach to grasp

Mesh:

Year:  2017        PMID: 29357477      PMCID: PMC5966743          DOI: 10.1152/jn.00982.2016

Source DB:  PubMed          Journal:  J Neurophysiol        ISSN: 0022-3077            Impact factor:   2.714


  45 in total

1.  Reorganization in primary motor cortex of primates with long-standing therapeutic amputations.

Authors:  C W Wu; J H Kaas
Journal:  J Neurosci       Date:  1999-09-01       Impact factor: 6.167

2.  Closed-loop decoder adaptation on intermediate time-scales facilitates rapid BMI performance improvements independent of decoder initialization conditions.

Authors:  Amy L Orsborn; Siddharth Dangi; Helene G Moorman; Jose M Carmena
Journal:  IEEE Trans Neural Syst Rehabil Eng       Date:  2012-07       Impact factor: 3.802

3.  Development of prehension movements in children: a kinematic study.

Authors:  J P Kuhtz-Buschbeck; H Stolze; K Jöhnk; A Boczek-Funcke; M Illert
Journal:  Exp Brain Res       Date:  1998-10       Impact factor: 1.972

4.  Dynamic organization of primary motor cortex output to target muscles in adult rats. I. Long-term patterns of reorganization following motor or mixed peripheral nerve lesions.

Authors:  J N Sanes; S Suner; J P Donoghue
Journal:  Exp Brain Res       Date:  1990       Impact factor: 1.972

5.  Adaptive decoding for brain-machine interfaces through Bayesian parameter updates.

Authors:  Zheng Li; Joseph E O'Doherty; Mikhail A Lebedev; Miguel A L Nicolelis
Journal:  Neural Comput       Date:  2011-09-15       Impact factor: 2.026

Review 6.  Neuroprosthetic technology for individuals with spinal cord injury.

Authors:  Jennifer L Collinger; Stephen Foldes; Tim M Bruns; Brian Wodlinger; Robert Gaunt; Douglas J Weber
Journal:  J Spinal Cord Med       Date:  2013-07       Impact factor: 1.985

7.  Rapid reorganization of adult rat motor cortex somatic representation patterns after motor nerve injury.

Authors:  J N Sanes; S Suner; J F Lando; J P Donoghue
Journal:  Proc Natl Acad Sci U S A       Date:  1988-03       Impact factor: 11.205

8.  Cortical representation of ipsilateral arm movements in monkey and man.

Authors:  Karunesh Ganguly; Lavi Secundo; Gireeja Ranade; Amy Orsborn; Edward F Chang; Dragan F Dimitrov; Jonathan D Wallis; Nicholas M Barbaro; Robert T Knight; Jose M Carmena
Journal:  J Neurosci       Date:  2009-10-14       Impact factor: 6.167

Review 9.  Brain-machine interfaces: computational demands and clinical needs meet basic neuroscience.

Authors:  Ferdinando A Mussa-Ivaldi; Lee E Miller
Journal:  Trends Neurosci       Date:  2003-06       Impact factor: 13.837

10.  Neural constraints on learning.

Authors:  Patrick T Sadtler; Kristin M Quick; Matthew D Golub; Steven M Chase; Stephen I Ryu; Elizabeth C Tyler-Kabara; Byron M Yu; Aaron P Batista
Journal:  Nature       Date:  2014-08-28       Impact factor: 49.962

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  3 in total

Review 1.  Brain-Machine Interfaces: Powerful Tools for Clinical Treatment and Neuroscientific Investigations.

Authors:  Marc W Slutzky
Journal:  Neuroscientist       Date:  2018-05-17       Impact factor: 7.519

2.  Responses of neurons in the rostral ventrolateral medulla of conscious cats to anticipated and passive movements.

Authors:  Derek M Miller; Asmita Joshi; Emmanuel T Kambouroglos; Isaiah C Engstrom; John P Bielanin; Samuel R Wittman; Andrew A McCall; Susan M Barman; Bill J Yates
Journal:  Am J Physiol Regul Integr Comp Physiol       Date:  2020-01-15       Impact factor: 3.619

3.  Using Coherence-based spectro-spatial filters for stimulus features prediction from electro-corticographic recordings.

Authors:  Jaime Delgado Saa; Andy Christen; Stephanie Martin; Brian N Pasley; Robert T Knight; Anne-Lise Giraud
Journal:  Sci Rep       Date:  2020-05-06       Impact factor: 4.379

  3 in total

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