Choice of Contact Points Modulates Sensorimotor Cortical Interactions for Dexterous Manipulation

Humans are unique in their ability to perform dexterous object manipulation in a wide variety of scenarios. However, previous work has used a grasping context that predominantly elicits memory-based control of digit forces by constraining where the object should be grasped. For this ‘constrained’ grasping context, primary motor cortex (M1) is involved in storage and retrieval of digit forces used in previous manipulations. In contrast, when choice of digit contact points is allowed (‘unconstrained’ grasping), behavioral studies revealed that forces are adjusted, on a trial-to-trial basis, as a function of digit position. This suggests a role of online feedback that detects digit position, rather than memory, for force control. However, despite the ubiquitous nature of unconstrained hand-object interactions in activities of daily living, the underlying neural mechanisms are unknown. Using non-invasive brain stimulation and electroencephalography, we found the role of M1 to be sensitive to grasping condition. While confirming the role of M1 in storing and retrieving learned digit forces and position in ‘constrained’ grasping, we also found that M1 is involved in modulating digit forces to digit position in unconstrained grasping. Furthermore, we found that digit force modulation to position relies on sensorimotor integration mediated by primary sensory cortex (S1) and M1. This finding supports the notion of a greater contribution of somatosensory feedback of digit position in unconstrained grasping. We conclude that the relative contribution of memory and online feedback based on whether contact points are constrained or unconstrained modulates sensorimotor cortical interactions for dexterous manipulation.

[1]  U. Castiello The neuroscience of grasping , 2005, Nature Reviews Neuroscience.

[2]  H. Yumiya,et al.  Peripheral input pathways to the monkey motor cortex , 1980, Experimental Brain Research.

[3]  Marco Santello,et al.  Transfer of Learned Manipulation following Changes in Degrees of Freedom , 2011, The Journal of Neuroscience.

[4]  S. Swinnen,et al.  Frequency-dependent effects of muscle tendon vibration on corticospinal excitability: a TMS study , 2003, Experimental Brain Research.

[5]  Marco Santello,et al.  On neuromechanical approaches for the study of biological and robotic grasp and manipulation , 2017, Journal of NeuroEngineering and Rehabilitation.

[6]  K. J. Cole,et al.  Sensory-motor coordination during grasping and manipulative actions , 1992, Current Opinion in Neurobiology.

[7]  Philippe A. Chouinard,et al.  Role of the Primary Motor and Dorsal Premotor Cortices in the Anticipation of Forces during Object Lifting , 2005, The Journal of Neuroscience.

[8]  Marco Santello,et al.  Choice of Contact Points during Multidigit Grasping: Effect of Predictability of Object Center of Mass Location , 2007, The Journal of Neuroscience.

[9]  Richard M. Leahy,et al.  Brainstorm: A User-Friendly Application for MEG/EEG Analysis , 2011, Comput. Intell. Neurosci..

[10]  M. Santello,et al.  Anticipatory Control of Grasping: Independence of Sensorimotor Memories for Kinematics and Kinetics , 2008, The Journal of Neuroscience.

[11]  Stephen H Scott,et al.  Distributed task-specific processing of somatosensory feedback for voluntary motor control , 2016, eLife.

[12]  Lee E Miller,et al.  Responses of somatosensory area 2 neurons to actively and passively generated limb movements. , 2013, Journal of neurophysiology.

[13]  J. Rothwell,et al.  Theta Burst Stimulation of the Human Motor Cortex , 2005, Neuron.

[14]  Mackenzie W. Mathis,et al.  Somatosensory Cortex Plays an Essential Role in Forelimb Motor Adaptation in Mice , 2017, Neuron.

[15]  Karl J. Friston,et al.  Canonical Microcircuits for Predictive Coding , 2012, Neuron.

[16]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[17]  Matteo Bianchi,et al.  Hand synergies: Integration of robotics and neuroscience for understanding the control of biological and artificial hands. , 2016, Physics of life reviews.

[18]  Anil K. Seth,et al.  The MVGC multivariate Granger causality toolbox: A new approach to Granger-causal inference , 2014, Journal of Neuroscience Methods.

[19]  K. J. Cole,et al.  Memory representations underlying motor commands used during manipulation of common and novel objects. , 1993, Journal of neurophysiology.

[20]  G Schlaug,et al.  Repetitive TMS of the motor cortex improves ipsilateral sequential simple finger movements , 2004, Neurology.

[21]  M. Davare,et al.  Temporal Dissociation between Hand Shaping and Grip Force Scaling in the Anterior Intraparietal Area , 2007, The Journal of Neuroscience.

[22]  H. Forssberg,et al.  Lighter or Heavier Than Predicted: Neural Correlates of Corrective Mechanisms during Erroneously Programmed Lifts , 2006, The Journal of Neuroscience.

[23]  J. Napier The prehensile movements of the human hand. , 1956, The Journal of bone and joint surgery. British volume.

[24]  R. Lemon Descending pathways in motor control. , 2008, Annual review of neuroscience.

[25]  Scott T. Grafton The cognitive neuroscience of prehension: recent developments , 2010, Experimental Brain Research.

[26]  S. Washburn,et al.  Tools and human evolution. , 1960, Scientific American.

[27]  Laurentius Huber,et al.  High-Resolution CBV-fMRI Allows Mapping of Laminar Activity and Connectivity of Cortical Input and Output in Human M1 , 2017, Neuron.

[28]  M. T. Wallace,et al.  Visual, auditory and somatosensory convergence in output neurons of the cat superior colliculus: multisensory properties of the tecto-reticulo-spinal projection , 2005, Experimental Brain Research.

[29]  H. Asanuma,et al.  Peripheral afferent inputs to the forelimb area of the monkey motor cortex: Input-output relations , 2004, Experimental Brain Research.

[30]  E. Wassermann,et al.  A safety screening questionnaire for transcranial magnetic stimulation , 2001, Clinical Neurophysiology.

[31]  R. Johansson,et al.  Programmed and triggered actions to rapid load changes during precision grip , 2004, Experimental Brain Research.

[32]  M. Arbib,et al.  Dorsal Premotor Cortex and Conditional Movement Selection: A PET Functional Mapping Study , 1998 .

[33]  Terrence J. Sejnowski,et al.  Independent Component Analysis Using an Extended Infomax Algorithm for Mixed Subgaussian and Supergaussian Sources , 1999, Neural Computation.

[34]  Howard Poizner,et al.  Anticipatory Modulation of Digit Placement for Grasp Control Is Affected by Parkinson's Disease , 2010, PloS one.

[35]  Marco Santello,et al.  Extraction of Time and Frequency Features From Grip Force Rates During Dexterous Manipulation , 2015, IEEE Transactions on Biomedical Engineering.

[36]  H. Forssberg,et al.  Differential fronto-parietal activation depending on force used in a precision grip task: an fMRI study. , 2001, Journal of neurophysiology.

[37]  Richard M. Leahy,et al.  BrainSuite: An Automated Cortical Surface Identification Tool , 2000, MICCAI.

[38]  Marco Davare,et al.  Interactions between areas of the cortical grasping network , 2011, Current Opinion in Neurobiology.

[39]  Marco Santello,et al.  Manipulation after object rotation reveals independent sensorimotor memory representations of digit positions and forces. , 2010, Journal of neurophysiology.

[40]  H. Topka,et al.  Deficits of predictive grip force control during object manipulation in acute stroke , 2003, Journal of Neurology.

[41]  S. Boniface,et al.  Magnetic brain stimulation with a double coil: the importance of coil orientation. , 1992, Electroencephalography and clinical neurophysiology.

[42]  S. E. Stewart The Polyoma Virus , 1960 .

[43]  R. S. Johansson,et al.  Roles of glabrous skin receptors and sensorimotor memory in automatic control of precision grip when lifting rougher or more slippery objects , 2004, Experimental Brain Research.

[44]  D. Wolpert,et al.  High‐frequency repetitive transcranial magnetic stimulation over the hand area of the primary motor cortex disturbs predictive grip force scaling , 2005, The European journal of neuroscience.

[45]  J. Randall Flanagan,et al.  Coding and use of tactile signals from the fingertips in object manipulation tasks , 2009, Nature Reviews Neuroscience.

[46]  L. Fadiga,et al.  Precision grasping in humans: from motor control to cognition , 2007, Current Opinion in Neurobiology.

[47]  Jody C. Culham,et al.  Human neuroimaging reveals the subcomponents of grasping, reaching and pointing actions , 2018, Cortex.

[48]  M. Davare,et al.  Behavioral / Systems / Cognitive Dissociating the Role of Ventral and Dorsal Premotor Cortex in Precision Grasping , 2018 .

[49]  Ivan Toni,et al.  Parieto-Frontal Connectivity during Visually Guided Grasping , 2007, The Journal of Neuroscience.

[50]  A. E. Casale,et al.  Motor Cortex Feedback Influences Sensory Processing by Modulating Network State , 2013, Neuron.

[51]  R. Johansson,et al.  Factors influencing the force control during precision grip , 2004, Experimental Brain Research.

[52]  Marco Santello,et al.  Neural Representations of Sensorimotor Memory- and Digit Position-Based Load Force Adjustments Before the Onset of Dexterous Object Manipulation , 2018, The Journal of Neuroscience.

[53]  O. Jensen,et al.  Shaping Functional Architecture by Oscillatory Alpha Activity: Gating by Inhibition , 2010, Front. Hum. Neurosci..

[54]  R. Johansson,et al.  Corticospinal control during reach, grasp, and precision lift in man , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[55]  R. Johansson,et al.  Predictive feed-forward sensory control during grasping and manipulation in man , 1993 .

[56]  Sarah E. Criscimagna-Hemminger,et al.  Contributions of the motor cortex to adaptive control of reaching depend on the perturbation schedule. , 2011, Cerebral cortex.

[57]  R. Johansson,et al.  Independent control of human finger‐tip forces at individual digits during precision lifting. , 1992, The Journal of physiology.

[58]  R. Johansson,et al.  Cortical activity in precision- versus power-grip tasks: an fMRI study. , 2000, Journal of neurophysiology.

[59]  Marco Santello,et al.  Sensorimotor uncertainty modulates corticospinal excitability during skilled object manipulation , 2019, Journal of neurophysiology.

[60]  R. Ilmoniemi,et al.  Interpreting magnetic fields of the brain: minimum norm estimates , 2006, Medical and Biological Engineering and Computing.

[61]  Marco Santello,et al.  Retention and interference of learned dexterous manipulation: interaction between multiple sensorimotor processes. , 2015, Journal of neurophysiology.

[62]  J R Wolpaw,et al.  Amplitude of responses to perturbation in primate sensorimotor cortex as a function of task. , 1980, Journal of neurophysiology.

[63]  M W Marzke,et al.  Precision grips, hand morphology, and tools. , 1997, American journal of physical anthropology.

[64]  John C Rothwell,et al.  Effect of physiological activity on an NMDA-dependent form of cortical plasticity in human. , 2008, Cerebral cortex.

[65]  Disruption of Activity in the Ventral Premotor But Not the Anterior Intraparietal Area Interferes with On-Line Correction to a Haptic Perturbation during Grasping , 2015, The Journal of Neuroscience.

[66]  Alexander T. Sack,et al.  Time- and Task-Dependent Non-Neural Effects of Real and Sham TMS , 2013, PloS one.

[67]  M. Santello,et al.  Corticospinal excitability underlying digit force planning for grasping in humans. , 2014, Journal of neurophysiology.

[68]  M. Ridding,et al.  Role of the primary motor and sensory cortex in precision grasping: a transcranial magnetic stimulation study , 2008, The European journal of neuroscience.

[69]  P. Suñé,et al.  Positive Outcomes Influence the Rate and Time to Publication, but Not the Impact Factor of Publications of Clinical Trial Results , 2013, PloS one.

[70]  A. Nelson,et al.  Current direction specificity of continuous theta-burst stimulation in modulating human motor cortex excitability when applied to somatosensory cortex , 2012, Neuroreport.

[71]  J. Szentágothai Anatomical considerations on monosynaptic reflex arcs. , 1948, Journal of neurophysiology.

[72]  H Asanuma,et al.  Information processing within the motor cortex. II. Intracortical connections between neurons receiving somatosensory cortical input and motor output neurons of the cortex , 1994, The Journal of comparative neurology.

[73]  W. Staines,et al.  Continuous Theta Burst Stimulation of the Supplementary Motor Area: Effect Upon Perception and Somatosensory and Motor Evoked Potentials , 2013, Brain Stimulation.

[74]  P. Bernier,et al.  Disruption of M1 Activity during Performance Plateau Impairs Consolidation of Motor Memories , 2017, The Journal of Neuroscience.

[75]  M. Santello,et al.  Anticipatory Planning and Control of Grasp Positions and Forces for Dexterous Two-Digit Manipulation , 2010, The Journal of Neuroscience.

[76]  T. Hoque,et al.  Two phases of interhemispheric inhibition between motor related cortical areas and the primary motor cortex in human. , 2009, Cerebral cortex.

[77]  Scott T. Grafton,et al.  Virtual lesions of the anterior intraparietal area disrupt goal-dependent on-line adjustments of grasp , 2005, Nature Neuroscience.

[78]  Gabriel Baud-Bovy,et al.  Neural bases of hand synergies , 2013, Front. Comput. Neurosci..

[79]  Karl J. Friston,et al.  LFP and oscillations—what do they tell us? , 2015, Current Opinion in Neurobiology.

[80]  Bart Vanrumste,et al.  Journal of Neuroengineering and Rehabilitation Open Access Review on Solving the Inverse Problem in Eeg Source Analysis , 2022 .

[81]  Per B. Brockhoff,et al.  lmerTest Package: Tests in Linear Mixed Effects Models , 2017 .

[82]  Michael J. Martinez,et al.  Bias between MNI and Talairach coordinates analyzed using the ICBM‐152 brain template , 2007, Human brain mapping.

[83]  M. Jeannerod,et al.  Impairment of grasping movements following a bilateral posterior parietal lesion , 1994, Neuropsychologia.