Synchronous Neural Oscillation Between the Right Inferior Fronto-Parietal Cortices Contributes to Body Awareness

The right inferior fronto-parietal network monitors the current status of the musculoskeletal system and builds-up and updates our postural model. The kinesthetic illusion induced by tendon vibration has been utilized in experiments on the modulation of body awareness. The right inferior fronto-parietal cortices activate during the kinesthetic illusion. We aimed to determine the relationship between the right inferior fronto-parietal cortices and body awareness by applying transcranial alternating current stimulation (tACS) to exogenously modulate oscillatory neural activity in the right fronto-parietal cortices during the kinesthetic illusion. Sixteen young adults participated in this study. We counterbalanced the order in which participants received the three types of tACS (55 Hz enveloped by 6 Hz; synchronous, desynchronous, and sham) across the subjects. The illusory movement perception induced by tendon vibration of the left extensor carpi ulnaris muscle was assessed before and during tACS. Application of synchronous tACS over the right inferior fronto-parietal cortices significantly increased kinesthetic illusion compared with sham tACS. The kinesthetic illusion during desynchronous tACS decreased from baseline. There was no change in vibration sensation during any tACS condition. The modulation of oscillatory brain activity between the right fronto-parietal cortices alters the illusory movement perception without altering actual vibration sensation. tACS over the right inferior fronto-parietal cortices is considered to modulate the neural processing involved in updating the postural model when the stimulated muscle spindle sends kinesthetic signals. This is the first study that reveals that rhythmic communication between the right inferior fronto-parietal cortices has a causal role in body awareness.

[1]  D. McCloskey,et al.  Proprioceptive Illusions Induced by Muscle Vibration: Contribution by Muscle Spindles to Perception? , 1972, Science.

[2]  D. Burke,et al.  The responses of human muscle spindle endings to vibration of non‐contracting muscles. , 1976, The Journal of physiology.

[3]  B. Edin,et al.  Dynamic response of human muscle spindle afferents to stretch. , 1990, Journal of neurophysiology.

[4]  S. Aglioti,et al.  The body in the brain: neural bases of corporeal awareness , 1997, Trends in Neurosciences.

[5]  E. Ribot-Ciscar,et al.  Ago-antagonist muscle spindle inputs contribute together to joint movement coding in man , 1998, Brain Research.

[6]  K. Zilles,et al.  Illusory Arm Movements Activate Cortical Motor Areas: A Positron Emission Tomography Study , 1999, The Journal of Neuroscience.

[7]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[8]  J. Roll,et al.  Kinaesthetic role of muscle afferents in man, studied by tendon vibration and microneurography , 2004, Experimental Brain Research.

[9]  J. Roll,et al.  Alteration of proprioceptive messages induced by tendon vibration in man: a microneurographic study , 2004, Experimental Brain Research.

[10]  Leslie G. Ungerleider,et al.  Dominance of the right hemisphere and role of area 2 in human kinesthesia. , 2005, Journal of neurophysiology.

[11]  G. Vallar,et al.  Shared Cortical Anatomy for Motor Awareness and Motor Control , 2005, Science.

[12]  D. Louis Collins,et al.  Symmetric Atlasing and Model Based Segmentation: An Application to the Hippocampus in Older Adults , 2006, MICCAI.

[13]  M. Berger,et al.  High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex , 2006, Science.

[14]  M. Tsakiris My body in the brain: A neurocognitive model of body-ownership , 2010, Neuropsychologia.

[15]  O. Blanke,et al.  Multi-Sensory and Sensorimotor Foundation of Bodily Self-Consciousness – An Interdisciplinary Approach , 2011, Front. Psychology.

[16]  J. Changeux,et al.  Experimental and Theoretical Approaches to Conscious Processing , 2011, Neuron.

[17]  M. Catani,et al.  A lateralized brain network for visuospatial attention , 2011, Nature Neuroscience.

[18]  O. Blanke Multisensory brain mechanisms of bodily self-consciousness , 2012, Nature Reviews Neuroscience.

[19]  M. Catani,et al.  Monkey to human comparative anatomy of the frontal lobe association tracts , 2012, Cortex.

[20]  A. Engel,et al.  Antiphasic 40 Hz Oscillatory Current Stimulation Affects Bistable Motion Perception , 2013, Brain Topography.

[21]  C. Herrmann,et al.  Transcranial alternating current stimulation: a review of the underlying mechanisms and modulation of cognitive processes , 2013, Front. Hum. Neurosci..

[22]  C. Assaiante,et al.  Boosted activation of right inferior frontoparietal network: A basis for illusory movement awareness , 2014, Human brain mapping.

[23]  J. Honoré,et al.  Functional neuro-anatomy of egocentric versus allocentric space representation , 2014, Neurophysiologie Clinique/Clinical Neurophysiology.

[24]  S. Marinakis,et al.  Experimental and theoretical approaches , 2015 .

[25]  M. Grueschow,et al.  The precision of value-based choices depends causally on fronto-parietal phase coupling , 2015, Nature Communications.

[26]  M. Thiebaut de Schotten,et al.  Atlasing the frontal lobe connections and their variability due to age and education: a spherical deconvolution tractography study , 2015, Brain Structure and Function.

[27]  Sukhvinder S. Obhi,et al.  Task-dependent and distinct roles of the temporoparietal junction and inferior frontal cortex in the control of imitation , 2014, Social cognitive and affective neuroscience.

[28]  E. Naito,et al.  Body representations in the human brain revealed by kinesthetic illusions and their essential contributions to motor control and corporeal awareness , 2016, Neuroscience Research.

[29]  Qiang Wang,et al.  The Role of the Frontal and Parietal Cortex in Proactive and Reactive Inhibitory Control: A Transcranial Direct Current Stimulation Study , 2016, Journal of Cognitive Neuroscience.

[30]  E. Naito,et al.  Importance of human right inferior frontoparietal network connected by inferior branch of superior longitudinal fasciculus tract in corporeal awareness of kinesthetic illusory movement , 2016, Cortex.

[31]  Robert Leech,et al.  Externally induced frontoparietal synchronization modulates network dynamics and enhances working memory performance , 2017, eLife.

[32]  Kristoffer Hougaard Madsen,et al.  How to target inter-regional phase synchronization with dual-site Transcranial Alternating Current Stimulation , 2017, NeuroImage.

[33]  M. Asada,et al.  Development of Right-hemispheric Dominance of Inferior Parietal Lobule in Proprioceptive Illusion Task , 2017, Cerebral cortex.

[34]  C. Herrmann,et al.  Non-invasive Brain Stimulation: A Paradigm Shift in Understanding Brain Oscillations , 2018, Front. Hum. Neurosci..

[35]  Melanie Wilke,et al.  Probing the Link Between Perception and Oscillations: Lessons from Transcranial Alternating Current Stimulation , 2019, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[36]  Yu Huang,et al.  Realistic volumetric-approach to simulate transcranial electric stimulation—ROAST—a fully automated open-source pipeline , 2019, Journal of neural engineering.