title: Engagement of the Rat Hindlimb Motor Cortex across Natural Locomotor Behaviors.
abstract: Contrary to cats and primates, cortical contribution to hindlimb locomotor movements is not critical in rats. However, the importance of the motor cortex to regain locomotion after neurological disorders in rats suggests that cortical engagement in hindlimb motor control may depend on the behavioral context. To investigate this possibility, we recorded whole-body kinematics, muscle synergies, and hindlimb motor cortex modulation in freely moving rats performing a range of natural locomotor procedures. We found that the activation of hindlimb motor cortex preceded gait initiation. During overground locomotion, the motor cortex exhibited consistent neuronal population responses that were synchronized with the spatiotemporal activation of hindlimb motoneurons. Behaviors requiring enhanced muscle activity or skilled paw placement correlated with substantial adjustment in neuronal population responses. In contrast, all rats exhibited a reduction of cortical activity during more automated behavior, such as stepping on a treadmill. Despite the facultative role of the motor cortex in the production of locomotion in rats, these results show that the encoding of hindlimb features in motor cortex dynamics is comparable in rats and cats. However, the extent of motor cortex modulations appears linked to the degree of volitional engagement and complexity of the task, reemphasizing the importance of goal-directed behaviors for motor control studies, rehabilitation, and neuroprosthetics.
  
  
  
  We mapped the neuronal population responses in the hindlimb motor cortex to hindlimb kinematics and hindlimb muscle synergies across a spectrum of natural locomotion behaviors. Robust task-specific neuronal population responses revealed that the rat motor cortex displays similar modulation as other mammals during locomotion. However, the reduced motor cortex activity during more automated behaviors suggests a relationship between the degree of engagement and task complexity. This relationship emphasizes the importance of the behavioral procedure to engage the motor cortex during motor control studies, gait rehabilitation, and locomotor neuroprosthetic developments in rats.
authors.affiliation: Bertarelli Foundation Chair in Translational Neuroengineering, Center for Neuroprosthetics and Institute of Bioengineering, Ecole Polytechnique Federale de Lausanne (EPFL), Lausanne 1005, Switzerland, jack.digiovanna@gmail.com gregoire.courtine@epfl.ch.
authors.forename: Jack
authors.identifier: 0000-0002-7757-4120
authors.initials: J
authors.lastname: DiGiovanna
authors.affiliation: International Paraplegic Foundation Chair Spinal Cord Repair, Center for Neuroprosthetics and Brain Mind Institute, Swiss Federal Institute of Technology (EPFL), Lausanne 1015, Switzerland, MOVE Research Institute Amsterdam, Department of Human Movement Sciences, VU University Amsterdam, Amsterdam 1081 HV, The Netherlands.
authors.forename: Nadia
authors.identifier: 0000-0003-2312-915X
authors.initials: N
authors.lastname: Dominici
authors.affiliation: International Paraplegic Foundation Chair Spinal Cord Repair, Center for Neuroprosthetics and Brain Mind Institute, Swiss Federal Institute of Technology (EPFL), Lausanne 1015, Switzerland.
authors.forename: Lucia
authors.initials: L
authors.lastname: Friedli
authors.affiliation: Bertarelli Foundation Chair in Translational Neuroengineering, Center for Neuroprosthetics and Institute of Bioengineering, Ecole Polytechnique Federale de Lausanne (EPFL), Lausanne 1005, Switzerland, Translational Neural Engineering Area, The BioRobotics Institute, Scuola Superiore Sant'Anna, Pisa 56127, Italy, and.
authors.forename: Jacopo
authors.identifier: 0000-0003-3184-994X
authors.initials: J
authors.lastname: Rigosa
authors.affiliation: International Paraplegic Foundation Chair Spinal Cord Repair, Center for Neuroprosthetics and Brain Mind Institute, Swiss Federal Institute of Technology (EPFL), Lausanne 1015, Switzerland.
authors.forename: Simone
authors.initials: S
authors.lastname: Duis
authors.affiliation: International Paraplegic Foundation Chair Spinal Cord Repair, Center for Neuroprosthetics and Brain Mind Institute, Swiss Federal Institute of Technology (EPFL), Lausanne 1015, Switzerland.
authors.forename: Julie
authors.initials: J
authors.lastname: Kreider
authors.affiliation: International Paraplegic Foundation Chair Spinal Cord Repair, Center for Neuroprosthetics and Brain Mind Institute, Swiss Federal Institute of Technology (EPFL), Lausanne 1015, Switzerland.
authors.forename: Janine
authors.initials: J
authors.lastname: Beauparlant
authors.affiliation: International Paraplegic Foundation Chair Spinal Cord Repair, Center for Neuroprosthetics and Brain Mind Institute, Swiss Federal Institute of Technology (EPFL), Lausanne 1015, Switzerland.
authors.forename: Rubia
authors.initials: R
authors.lastname: van den Brand
authors.affiliation: Department of Public Health, Experimental and Forensic Medicine, University of Pavia, and Fondazione Salvatore Maugeri (IRCCS), Centro Studi Attività Motorie (CSAM), Pavia 27100, Italy.
authors.forename: Marco
authors.identifier: 0000-0002-0630-0819
authors.initials: M
authors.lastname: Schieppati
authors.affiliation: Bertarelli Foundation Chair in Translational Neuroengineering, Center for Neuroprosthetics and Institute of Bioengineering, Ecole Polytechnique Federale de Lausanne (EPFL), Lausanne 1005, Switzerland, Translational Neural Engineering Area, The BioRobotics Institute, Scuola Superiore Sant'Anna, Pisa 56127, Italy, and.
authors.forename: Silvestro
authors.identifier: 0000-0003-4396-8217
authors.initials: S
authors.lastname: Micera
authors.affiliation: International Paraplegic Foundation Chair Spinal Cord Repair, Center for Neuroprosthetics and Brain Mind Institute, Swiss Federal Institute of Technology (EPFL), Lausanne 1015, Switzerland, jack.digiovanna@gmail.com gregoire.courtine@epfl.ch.
authors.forename: Grégoire
authors.identifier: 0000-0002-5744-4142
authors.initials: G
authors.lastname: Courtine
mesh_terms: D000818:Animals; D001522:Behavior, Animal / Q000502:physiology; D001696:Biomechanical Phenomena; D004576:Electromyography; D005260:Female; D005684:Gait / Q000502:physiology; D006614:Hindlimb / Q000294:innervation* / Q000502:physiology*; D008124:Locomotion / Q000502:physiology*; D009044:Motor Cortex / Q000502:physiology*; D018482:Muscle, Skeletal / Q000294:innervation / Q000502:physiology; D009434:Neural Pathways / Q000502:physiology; D011712:Pyramidal Tracts / Q000166:cytology / Q000502:physiology; D051381:Rats; D011917:Rats, Inbred Lew
keywords: kinematics; locomotion; motor cortex; muscle synergies; neural ensemble; rat