Neural circuits activated by error amplification and haptic guidance training techniques during performance of a timing-based motor task by healthy individuals

To promote motor learning, robotic devices have been used to improve subjects’ performance by guiding desired movements (haptic guidance—HG) or by artificially increasing movement errors to foster a more rapid learning (error amplification—EA). To better understand the neurophysiological basis of motor learning, a few studies have evaluated brain regions activated during EA/HG, but none has compared both approaches. The goal of this study was to investigate using fMRI which brain networks were activated during a single training session of HG/EA in healthy adults learning to play a computerized pinball-like timing task. Subjects had to trigger a robotic device by flexing their wrist at the correct timing to activate a virtual flipper and hit a falling ball towards randomly positioned targets. During training with HG/EA, subjects’ timing errors were decreased/increased, respectively, by the robotic device to delay or accelerate their wrist movement. The results showed that at the beginning of the training period with HG/EA, an error-detection network, including cerebellum and angular gyrus, was activated, consistent with subjects recognizing discrepancies between their intended actions and the actual movement timing. At the end of the training period, an error-detection network was still present for EA, while a memory consolidation/automatization network (caudate head and parahippocampal gyrus) was activated for HG. The results indicate that training movement with various kinds of robotic input relies on different brain networks. Better understanding the neurophysiological underpinnings of brain processes during HG/EA could prove useful for optimizing rehabilitative movement training for people with different patterns of brain damage.

[1]  C. Fiebach,et al.  The role of left inferior frontal and superior temporal cortex in sentence comprehension: localizing syntactic and semantic processes. , 2003, Cerebral cortex.

[2]  J. Patton,et al.  Evaluation of robotic training forces that either enhance or reduce error in chronic hemiparetic stroke survivors , 2005, Experimental Brain Research.

[3]  W. Schultz Reward functions of the basal ganglia , 2016, Journal of Neural Transmission.

[4]  T. Komiyama,et al.  Circuit Mechanisms of Sensorimotor Learning , 2016, Neuron.

[5]  Shawn W. Ell,et al.  Learning robust cortico-cortical associations with the basal ganglia: An integrative review , 2015, Cortex.

[6]  H. Heuer,et al.  Robot assistance of motor learning: A neuro-cognitive perspective , 2015, Neuroscience & Biobehavioral Reviews.

[7]  M. Rugg,et al.  Ventral lateral parietal cortex and episodic memory retrieval , 2017, Cortex.

[8]  Eli Carmeli,et al.  Error augmentation as a possible technique for improving upper extremity motor performance after a stroke – a systematic review , 2016, Topics in stroke rehabilitation.

[9]  U. Halsband,et al.  Motor learning in man: A review of functional and clinical studies , 2006, Journal of Physiology-Paris.

[10]  C. Price The anatomy of language: a review of 100 fMRI studies published in 2009 , 2010, Annals of the New York Academy of Sciences.

[11]  Robert Teasell,et al.  Canadian stroke best practice recommendations: Stroke rehabilitation practice guidelines, update 2015 , 2016, International journal of stroke : official journal of the International Stroke Society.

[12]  Marc Jeannerod,et al.  Modulating the experience of agency: a positron emission tomography study , 2003, NeuroImage.

[13]  M. Guadagnoli,et al.  Challenge Point: A Framework for Conceptualizing the Effects of Various Practice Conditions in Motor Learning , 2004, Journal of motor behavior.

[14]  Alan C. Evans,et al.  A Specific Role for the Right Parahippocampal Gyrus in the Retrieval of Object-Location: A Positron Emission Tomography Study , 1996, Journal of Cognitive Neuroscience.

[15]  Josef P. Rauschecker,et al.  Wernicke’s area revisited: Parallel streams and word processing , 2013, Brain and Language.

[16]  Hélène Corriveau,et al.  A single robotic session that guides or increases movement error in survivors post-chronic stroke: which intervention is best to boost the learning of a timing task? , 2017, Disability and rehabilitation.

[17]  F. Chollet,et al.  Within-Session and Between-Session Reproducibility of Cerebral Sensorimotor Activation: A Test–Retest Effect Evidenced with Functional Magnetic Resonance Imaging , 2001, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[18]  N. Daw,et al.  Fronto-striatal organization: Defining functional and microstructural substrates of behavioural flexibility , 2016, Cortex.

[19]  G. Yue,et al.  Prolonged cognitive planning time, elevated cognitive effort, and relationship to coordination and motor control following stroke , 2006, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[20]  Rajesh K. Kana,et al.  Language and motor cortex response to comprehending accidental and intentional action sentences , 2015, Neuropsychologia.

[21]  Babak Shahbaba,et al.  Neural function, injury, and stroke subtype predict treatment gains after stroke , 2015, Annals of neurology.

[22]  Reza Shadmehr,et al.  Learning from Sensory and Reward Prediction Errors during Motor Adaptation , 2011, PLoS Comput. Biol..

[23]  Frans C. T. van der Helm,et al.  Influence of haptic guidance in learning a novel visuomotor task , 2009, Journal of Physiology-Paris.

[24]  M. Jeannerod,et al.  Perception of self-generated movement following left parietal lesion. , 1999, Brain : a journal of neurology.

[25]  David Luck,et al.  The right parahippocampal gyrus contributes to the formation and maintenance of bound information in working memory , 2010, Brain and Cognition.

[26]  G. Rizzolatti,et al.  Neural Circuits Underlying Imitation Learning of Hand Actions An Event-Related fMRI Study , 2004, Neuron.

[27]  David J. Turk,et al.  The angular gyrus computes action awareness representations. , 2008, Cerebral cortex.

[28]  G. Barker,et al.  Study design in fMRI: Basic principles , 2006, Brain and Cognition.

[29]  Donald Hedeker,et al.  Error Augmentation Enhancing Arm Recovery in Individuals With Chronic Stroke , 2014, Neurorehabilitation and neural repair.

[30]  Robert Riener,et al.  The effectiveness of robotic training depends on motor task characteristics , 2017, Experimental Brain Research.

[31]  John J. Foxe,et al.  The role of cingulate cortex in the detection of errors with and without awareness: a high‐density electrical mapping study , 2007, The European journal of neuroscience.

[32]  Matthew J. Crossley,et al.  Automaticity and multiple memory systems. , 2012, Wiley interdisciplinary reviews. Cognitive science.

[33]  Peter Wolf,et al.  The effect of haptic guidance and visual feedback on learning a complex tennis task , 2013, Experimental Brain Research.

[34]  R. Passingham,et al.  The Attentional Role of the Left Parietal Cortex: The Distinct Lateralization and Localization of Motor Attention in the Human Brain , 2001, Journal of Cognitive Neuroscience.

[35]  Kae Nakamura,et al.  Differential Reward Coding in the Subdivisions of the Primate Caudate during an Oculomotor Task , 2012, The Journal of Neuroscience.

[36]  M. Desmurget,et al.  Movement Intention After Parietal Cortex Stimulation in Humans , 2009, Science.

[37]  Michael F Land,et al.  Do we have an internal model of the outside world? , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[38]  S. Kiebel,et al.  Brain Representation of Active and Passive Movements , 1996, NeuroImage.

[39]  Ikuko Mukai,et al.  A role of right middle frontal gyrus in reorienting of attention: a case study , 2015, Front. Syst. Neurosci..

[40]  Sarah E. Criscimagna-Hemminger,et al.  Cerebellar Contributions to Reach Adaptation and Learning Sensory Consequences of Action , 2012, The Journal of Neuroscience.

[41]  David J. Reinkensmeyer,et al.  Comparison of error-amplification and haptic-guidance training techniques for learning of a timing-based motor task by healthy individuals , 2010, Experimental Brain Research.

[42]  W. Gehring,et al.  Neural Systems for Error Monitoring , 2007, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[43]  Hyoung F. Kim,et al.  Parallel basal ganglia circuits for voluntary and automatic behaviour to reach rewards. , 2015, Brain : a journal of neurology.

[44]  F Chollet,et al.  Neural Substrate for the Effects of Passive Training on Sensorimotor Cortical Representation: A Study with Functional Magnetic Resonance Imaging in Healthy Subjects , 2000, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[45]  Angela R. Laird,et al.  ALE meta-analysis of action observation and imitation in the human brain , 2010, NeuroImage.

[46]  Sung Tae Kim,et al.  Dynamic changes in the cortico-subcortical network during early motor learning. , 2010, NeuroRehabilitation.

[47]  C. Wan,et al.  Comparison of the reaction time of wrist flexion and extension between patients with stroke and age‐matched healthy subjects and correlation with clinical measures , 2013, Chinese medical journal.

[48]  R. Riener,et al.  Brain activation associated with active and passive lower limb stepping , 2014, Front. Hum. Neurosci..

[49]  Katharina N. Seidl-Rathkopf,et al.  Functions of the human frontoparietal attention network: Evidence from neuroimaging , 2015, Current Opinion in Behavioral Sciences.

[50]  Robert Riener,et al.  Effect of Error Augmentation on Brain Activation and Motor Learning of a Complex Locomotor Task , 2017, Front. Neurosci..

[51]  Yasmin L. Hashambhoy,et al.  Neural Correlates of Reach Errors , 2005, The Journal of Neuroscience.

[52]  P. Cavanagh,et al.  Opinion TRENDS in Cognitive Sciences Vol.11 No.5 The ‘when ’ pathway of the right parietal lobe , 2022 .

[53]  Robert Riener,et al.  The Effect of Haptic Guidance on Learning a Hybrid Rhythmic-Discrete Motor Task , 2015, IEEE Transactions on Haptics.

[54]  Lutz Jäncke,et al.  Motor and non-motor error and the influence of error magnitude on brain activity , 2010, Experimental Brain Research.

[55]  A. Georgopoulos Cognitive motor control: spatial and temporal aspects , 2002, Current Opinion in Neurobiology.

[56]  R. Riener,et al.  Learning a locomotor task: with or without errors? , 2014, Journal of NeuroEngineering and Rehabilitation.

[57]  John Peter Scholz,et al.  Timing variability of reach trajectories in left versus right hemisphere stroke , 2011, Brain Research.

[58]  P. Matthews,et al.  Identifying brain regions for integrative sensorimotor processing with ankle movements , 2005, Experimental Brain Research.

[59]  D. Reinkensmeyer,et al.  Review of control strategies for robotic movement training after neurologic injury , 2009, Journal of NeuroEngineering and Rehabilitation.

[60]  H. Johansson,et al.  Comparison of brain activity during different types of proprioceptive inputs: a positron emission tomography study , 2002, Experimental Brain Research.

[61]  Karl J. Friston,et al.  The Importance of Distributed Sampling in Blocked Functional Magnetic Resonance Imaging Designs , 2002, NeuroImage.

[62]  Ferdinando A. Mussa-Ivaldi,et al.  Robot-assisted adaptive training: custom force fields for teaching movement patterns , 2004, IEEE Transactions on Biomedical Engineering.

[63]  Margot J. Taylor,et al.  The centre of the brain: Topographical model of motor, cognitive, affective, and somatosensory functions of the basal ganglia , 2013, Human brain mapping.

[64]  R. Shadmehr,et al.  Neural correlates of motor memory consolidation. , 1997, Science.

[65]  Alexander Münchau,et al.  Investigating the human mirror neuron system by means of cortical synchronization during the imitation of biological movements , 2006, NeuroImage.

[66]  Done-Sik Yoo,et al.  Neural correlates related to action observation in expert archers , 2011, Behavioural Brain Research.

[67]  D.J. Reinkensmeyer,et al.  Robot-enhanced motor learning: accelerating internal model formation during locomotion by transient dynamic amplification , 2005, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[68]  P. Haggard,et al.  From action intentions to action effects: how does the sense of agency come about? , 2014, Front. Hum. Neurosci..

[69]  J. Krakauer,et al.  Sensory prediction errors drive cerebellum-dependent adaptation of reaching. , 2007, Journal of neurophysiology.

[70]  Jean-François Démonet,et al.  Electrostimulation mapping of comprehension of auditory and visual words , 2015, Cortex.

[71]  Robert Riener,et al.  A Reliability Study on Brain Activation During Active and Passive Arm Movements Supported by an MRI-Compatible Robot , 2014, Brain Topography.

[72]  Hélène Corriveau,et al.  Comparison of haptic guidance and error amplification robotic trainings for the learning of a timing-based motor task by healthy seniors , 2015, Front. Syst. Neurosci..

[73]  Jaime E. Duarte,et al.  Effects of robotically modulating kinematic variability on motor skill learning and motivation. , 2015, Journal of neurophysiology.

[74]  Simon B. Eickhoff,et al.  A quantitative meta-analysis and review of motor learning in the human brain , 2013, NeuroImage.

[75]  R. Colombo,et al.  Concurrent changes in shortening reaction latency and reaction time of forearm muscles in post-stroke patients , 2006, Neurological Sciences.

[76]  Angela Sirigu,et al.  Body and movement: Consciousness in the parietal lobes , 2010, Neuropsychologia.