Direct electrical stimulation of the premotor cortex shuts down awareness of voluntary actions

A challenge for neuroscience is to understand the conscious and unconscious processes underlying construction of willed actions. We investigated the neural substrate of human motor awareness during awake brain surgery. In a first experiment, awake patients performed a voluntary hand motor task and verbally monitored their real-time performance, while different brain areas were transiently impaired by direct electrical stimulation (DES). In a second experiment, awake patients retrospectively reported their motor performance after DES. Based on anatomo-clinical evidence from motor awareness disorders following brain damage, the premotor cortex (PMC) was selected as a target area and the primary somatosensory cortex (S1) as a control area. In both experiments, DES on both PMC and S1 interrupted movement execution, but only DES on PMC dramatically altered the patients’ motor awareness, making them unconscious of the motor arrest. These findings endorse PMC as a crucial hub in the anatomo-functional network of human motor awareness. Here, using electrical stimulation on patients undergoing awake brain surgery, the authors show that disruption of the premotor cortex makes patients unconscious of motor arrest. This finding suggests the premotor cortex is crucial for motor awareness.

[1]  Luca Viganò,et al.  Frontal pathways in cognitive control: direct evidence from intraoperative stimulation and diffusion tractography , 2019, Brain : a journal of neurology.

[2]  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.

[3]  Satrajit S. Ghosh,et al.  fMRI investigation of unexpected somatosensory feedback perturbation during speech , 2011, NeuroImage.

[4]  R. C. Macridis A review , 1963 .

[5]  A. Münchau,et al.  Inhibitory and facilitatory connectivity from ventral premotor to primary motor cortex in healthy humans at rest – A bifocal TMS study , 2009, Clinical Neurophysiology.

[6]  N. Soroker,et al.  Anosognosia for Hemiplegia in Stroke Rehabilitation , 2001, Neurorehabilitation and neural repair.

[7]  Francesca Garbarini,et al.  'Moving' a paralysed hand: bimanual coupling effect in patients with anosognosia for hemiplegia. , 2012, Brain : a journal of neurology.

[8]  J. Izawa,et al.  The cerebro-cerebellum: Could it be loci of forward models? , 2016, Neuroscience Research.

[9]  Marcello Gallucci,et al.  Monopolar high-frequency language mapping: can it help in the surgical management of gliomas? A comparative clinical study. , 2016, Journal of neurosurgery.

[10]  Ivan Toni,et al.  Movement-Specific Repetition Suppression in Ventral and Dorsal Premotor Cortex during Action Observation , 2009, Cerebral cortex.

[11]  Michael I. Jordan,et al.  An internal model for sensorimotor integration. , 1995, Science.

[12]  F. Baldissera,et al.  Cyclic h-reflex modulation in resting forearm related to contractions of foot movers, not to foot movement. , 2003, Journal of neurophysiology.

[13]  S. Blakemore,et al.  Action prediction in the cerebellum and in the parietal lobe , 2003, Experimental Brain Research.

[14]  F. Pessina,et al.  Preserving executive functions in nondominant frontal lobe glioma surgery: an intraoperative tool. , 2019, Journal of neurosurgery.

[15]  R. Sterzi,et al.  The physiology of motor delusions in anosognosia for hemiplegia: Implications for current models of motor awareness , 2014, Consciousness and Cognition.

[16]  F. Schmidt Meta-Analysis , 2008 .

[17]  A. Berti,et al.  Dissociations and similarities in motor intention and motor awareness: the case of anosognosia for hemiplegia and motor neglect , 2012, Journal of Neurology, Neurosurgery & Psychiatry.

[18]  A. Berti,et al.  From intention to perception: The case of anosognosia for hemiplegia , 2016, Neuropsychologia.

[19]  Andrew Simmons,et al.  Frontoparietal Tracts Linked to Lateralized Hand Preference and Manual Specialization , 2018, Cerebral cortex.

[20]  E Wyllie,et al.  Cortical electrical stimulation in humans. The negative motor areas. , 1995, Advances in neurology.

[21]  B. Libet,et al.  Time of conscious intention to act in relation to onset of cerebral activity (readiness-potential). The unconscious initiation of a freely voluntary act. , 1983 .

[22]  Luca Viganò,et al.  Direct Electrical Stimulation of Premotor Areas: Different Effects on Hand Muscle Activity during Object Manipulation , 2019, Cerebral cortex.

[23]  P. Haggard Conscious intention and motor cognition , 2005, Trends in Cognitive Sciences.

[24]  H. Shibasaki,et al.  Evidence for a wide distribution of negative motor areas in the perirolandic cortex , 2006, Clinical Neurophysiology.

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

[26]  Ronald R. Peeters,et al.  A human homologue of monkey F5c , 2015, NeuroImage.

[27]  P. Haggard,et al.  Neuroscience and Biobehavioral Reviews Intentional Inhibition in Human Action: the Power of 'no' , 2022 .

[28]  Matteo Bianchi,et al.  A synergy-based hand control is encoded in human motor cortical areas , 2016, eLife.

[29]  Luca Viganò,et al.  Anatomo-functional characterisation of the human “hand-knob”: A direct electrophysiological study , 2019, Cortex.

[30]  Enrica Fava,et al.  Assessment of the praxis circuit in glioma surgery to reduce the incidence of postoperative and long-term apraxia: a new intraoperative test. , 2018, Journal of neurosurgery.

[31]  Giuseppe Vallar,et al.  Anosognosia for motor and sensory deficits after unilateral brain damage: a review. , 2006, Restorative neurology and neuroscience.

[32]  R N Lemon,et al.  Functional Characterization of the Left Ventrolateral Premotor Cortex in Humans: A Direct Electrophysiological Approach , 2018, Cerebral cortex.

[33]  N. Beschin,et al.  VATA-M: VISUAL-ANALOGUE TEST ASSESSING ANOSOGNOSIA FOR MOTOR IMPAIRMENT , 2009, The Clinical neuropsychologist.

[34]  M. Desmurget,et al.  Selective Inhibition of Volitional Hand Movements after Stimulation of the Dorsoposterior Parietal Cortex in Humans , 2018, Current Biology.

[35]  A. Berti,et al.  To Move or Not to Move? Functional Role of Ventral Premotor Cortex in Motor Monitoring During Limb Immobilization , 2018, Cerebral cortex.

[36]  C. Papagno,et al.  INTRAOPERATIVE SUBCORTICAL LANGUAGETRACT MAPPING GUIDES SURGICAL REMOVALOF GLIOMAS INVOLVING SPEECH AREAS , 2007, Neurosurgery.

[37]  Antonella Castellano,et al.  Tailoring neurophysiological strategies with clinical context enhances resection and safety and expands indications in gliomas involving motor pathways. , 2014, Neuro-oncology.

[38]  P. Haggard,et al.  The role of motor intention in motor awareness: an experimental study on anosognosia for hemiplegia. , 2008, Brain : a journal of neurology.

[39]  B. Libet,et al.  Time of conscious intention to act in relation to onset of cerebral activity (readiness-potential). The unconscious initiation of a freely voluntary act. , 1983, Brain : a journal of neurology.

[40]  J. Baldo,et al.  Is relational reasoning dependent on language? A voxel-based lesion symptom mapping study , 2010, Brain and Language.

[41]  Marco Davare,et al.  Ventral premotor to primary motor cortical interactions during object-driven grasp in humans , 2009, Cortex.

[42]  Nadia Bolognini,et al.  “How Did I Make It?”: Uncertainty about Own Motor Performance after Inhibition of the Premotor Cortex , 2016, Journal of Cognitive Neuroscience.

[43]  A. Berti,et al.  Anosognosia for hemiplegia, neglect dyslexia, and drawing neglect: Clinical findings and theoretical considerations , 1996, Journal of the International Neuropsychological Society.

[44]  C. Morón,et al.  Transcranial Magnetic Stimulation Study , 2013 .

[45]  A. Berti,et al.  Anosognosia for hemianaesthesia: A voxel-based lesion-symptom mapping study , 2014, Cortex.

[46]  Scott T. Grafton,et al.  Role of the posterior parietal cortex in updating reaching movements to a visual target , 1999, Nature Neuroscience.

[47]  A. Fotopoulou,et al.  Explicit and implicit anosognosia or upper limb motor impairment , 2010, Neuropsychologia.

[48]  S. Forkel,et al.  Mentalizing the body: spatial and social cognition in anosognosia for hemiplegia , 2016, Brain : a journal of neurology.

[49]  M. Jeannerod,et al.  Limited conscious monitoring of motor performance in normal subjects , 1998, Neuropsychologia.

[50]  Carlotta Fossataro,et al.  The role of premotor and parietal cortex during monitoring of involuntary movement: A combined TMS and tDCS study , 2017, Cortex.

[51]  Ian Nimmo-Smith,et al.  Anosognosia for Plegia: Specificity, Extension, Partiality and Disunity of Bodily Unawareness , 2004, Cortex.

[52]  P. Vuilleumier,et al.  Anosognosia for hemiplegia: a clinical-anatomical prospective study. , 2010, Brain : a journal of neurology.

[53]  D. Levine,et al.  Babinski, J. (1914). Contribution to the Study of the Mental Disorders in Hemiplegia of Organic Cerebral Origin (Anosognosia). Translated by K.G. Langer & D.N. Levine Translated from the original Contribution à l'Étude des Troubles Mentaux dans l'Hémiplégie Organique Cérébrale (Anosognosie) , 2014, Cortex.

[54]  H. Duffau,et al.  A probabilistic map of negative motor areas of the upper limb and face: a brain stimulation study , 2019, Brain : a journal of neurology.

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

[56]  P. Strick,et al.  Frontal Lobe Inputs to the Digit Representations of the Motor Areas on the Lateral Surface of the Hemisphere , 2005, The Journal of Neuroscience.

[57]  Hans-Otto Karnath,et al.  Awareness of the Functioning of One's Own Limbs Mediated by the Insular Cortex? , 2005, The Journal of Neuroscience.

[58]  A. Berti,et al.  Invisible grasps: Grip interference in anosognosia for hemiplegia. , 2015, Neuropsychology.

[59]  R. Levy,et al.  Advanced lesion symptom mapping analyses and implementation as BCBtoolkit , 2017, bioRxiv.

[60]  Michel Thiebaut de Schotten,et al.  Short frontal lobe connections of the human brain , 2012, Cortex.

[61]  Daniel M. Corcos,et al.  Three-dimensional locations and boundaries of motor and premotor cortices as defined by functional brain imaging: A meta-analysis , 2006, NeuroImage.