fNIRS measure of transitive and intransitive gesture execution, observation and imagination in ecological setting: A pilot study

To explore the presence of differential cortical hemodynamic activations related to cognitive components of actions, we performed a fNIRS (functional Near-Infrared Spectroscopy) study during Observation (O), Execution (E) and Imagination (I) of complex and meaningful (transitive and intransitive) gestures in ecological setting. A pilot sample of 5 healthy adults underwent an event-related study consisting of these 3 different conditions, with O set as first and followed by a randomized presentation of E or I. fNIRS measurements were performed using a 24 channel array of optodes (8 light injectors and 8 detectors) placed over the contralateral central, centro-parietal, parietal and temporal areas. Results showed that the premotor (PMC) and the sensory-motor cortices (SM1) were recruited selectively during E, with levels of oxygenated hemoglobin (oxy-Hb) higher than the other conditions, while the posterior parietal cortex (PPC) showed increased oxy-Hb levels for both E and O. These data suggest that variations in hemodynamic responses can be attributed to different neural processes underpinning these tasks, with PMC and SM1 being more involved in action preparation and performance, and PPC prevalently dedicated to attentive processes related to the execution and observation of limb movements.

[1]  Tomohiro Ishizu,et al.  Motor activity and imagery modulate the body-selective region in the occipital–temporal area: A near-infrared spectroscopy study , 2009, Neuroscience Letters.

[2]  K. Kubota,et al.  Neurofeedback Using Real-Time Near-Infrared Spectroscopy Enhances Motor Imagery Related Cortical Activation , 2012, PloS one.

[3]  Gregory Króliczak,et al.  A common network in the left cerebral hemisphere represents planning of tool use pantomimes and familiar intransitive gestures at the hand-independent level. , 2009, Cerebral cortex.

[4]  J. Decety,et al.  Functional anatomy of execution, mental simulation, observation, and verb generation of actions: A meta‐analysis , 2001, Human brain mapping.

[5]  S. Jang,et al.  Cortical activation change induced by neuromuscular electrical stimulation during hand movements: a functional NIRS study , 2014, Journal of NeuroEngineering and Rehabilitation.

[6]  R. E. Passingham,et al.  Parietal cortex and movement II. Spatial representation , 1997, Experimental Brain Research.

[7]  Marco Iacoboni,et al.  Interhemispheric visuo-motor integration in humans: the role of the superior parietal cortex , 2004, Neuropsychologia.

[8]  Niels Birbaumer,et al.  Evidence for a different role of the ventral and dorsal medial prefrontal cortex for social reactive aggression: An interactive fMRI study , 2007, NeuroImage.

[9]  D. Kiper,et al.  Testing the potential of a virtual reality neurorehabilitation system during performance of observation, imagery and imitation of motor actions recorded by wireless functional near-infrared spectroscopy (fNIRS) , 2010, Journal of NeuroEngineering and Rehabilitation.

[10]  K. Shibuya The activity of the primary motor cortex ipsilateral to the exercising hand decreases during repetitive handgrip exercise , 2011, Physiological measurement.

[11]  Nadim Joni Shah,et al.  Prefrontal involvement in imitation learning of hand actions: Effects of practice and expertise , 2007, NeuroImage.

[12]  Christa Neuper,et al.  Does conscious intention to perform a motor act depend on slow prefrontal (de)oxyhemoglobin oscillations in the resting brain? , 2012, Neuroscience Letters.

[13]  C Neuper,et al.  Spatio-temporal differences in brain oxygenation between movement execution and imagery: a multichannel near-infrared spectroscopy study. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[14]  S. Jang,et al.  The cortical activation differences between proximal and distal joint movements of the upper extremities: a functional NIRS study. , 2013, NeuroRehabilitation.

[15]  S. Frey Tool use, communicative gesture and cerebral asymmetries in the modern human brain , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[16]  Prisca Stenneken,et al.  The human execution/observation matching system investigated with a complex everyday task: A functional near-infrared spectroscopy (fNIRS) study , 2012, Neuroscience Letters.

[17]  M. M. Richter,et al.  Event‐related functional near‐infrared spectroscopy (fNIRS) based on craniocerebral correlations: Reproducibility of activation? , 2007, Human brain mapping.

[18]  Roel M. Willems,et al.  When language meets action: the neural integration of gesture and speech. , 2007, Cerebral cortex.

[19]  E. DeYoe,et al.  Distinct Cortical Pathways for Processing Tool versus Animal Sounds , 2005, The Journal of Neuroscience.

[20]  Garrison W Cottrell,et al.  Observed, Executed, and Imagined Action Representations can be Decoded From Ventral and Dorsal Areas. , 2015, Cerebral cortex.

[21]  Sotaro Shimada,et al.  Modulation of motor area activity during observation of unnatural body movements , 2012, Brain and Cognition.

[22]  A. Goldman,et al.  Mirror neurons and the simulation theory of mind-reading , 1998, Trends in Cognitive Sciences.

[23]  Martin Wolf,et al.  Single-trial classification of motor imagery differing in task complexity: a functional near-infrared spectroscopy study , 2011, Journal of NeuroEngineering and Rehabilitation.

[24]  Ichiro Miyai,et al.  Frontal regions involved in learning of motor skill—A functional NIRS study , 2007, NeuroImage.

[25]  M. Jeannerod Neural Simulation of Action: A Unifying Mechanism for Motor Cognition , 2001, NeuroImage.

[26]  Silvia Erika Kober,et al.  Changes in hemodynamic signals accompanying motor imagery and motor execution of swallowing: A near-infrared spectroscopy study , 2014, NeuroImage.

[27]  R. Gentili,et al.  Functional near-infrared spectroscopy-based correlates of prefrontal cortical dynamics during a cognitive-motor executive adaptation task , 2013, Front. Hum. Neurosci..

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

[29]  R. Macwalter,et al.  A comparison of bilateral and unilateral upper-limb task training in early poststroke rehabilitation: a randomized controlled trial. , 2008, Archives of physical medicine and rehabilitation.

[30]  M Jeannerod,et al.  The hand and the object: the role of posterior parietal cortex in forming motor representations. , 1994, Canadian journal of physiology and pharmacology.

[31]  J. Cumming,et al.  The Functional Equivalence Between Movement Imagery, Observation, and Execution Influences Imagery Ability , 2011, Research quarterly for exercise and sport.

[32]  Nguyen Thanh Hai,et al.  Temporal hemodynamic classification of two hands tapping using functional near—infrared spectroscopy , 2013, Front. Hum. Neurosci..

[33]  E. Altenmüller,et al.  Transmodal Sensorimotor Networks during Action Observation in Professional Pianists , 2005, Journal of Cognitive Neuroscience.

[34]  Tony W. Wilson,et al.  Functional specialization within the supplementary motor area: A fNIRS study of bimanual coordination , 2014, NeuroImage.