Coordinated, multi-joint, fatigue-resistant feline stance produced with intrafascicular hind limb nerve stimulation

The production of graceful skeletal movements requires coordinated activation of multiple muscles that produce torques around multiple joints. The work described herein is focused on one such movement, stance, that requires coordinated activation of extensor muscles acting around the hip, knee and ankle joints. The forces evoked in these muscles by external stimulation all have a complex dependence on muscle length and shortening velocities, and some of these muscles are biarticular. In order to recreate sit-to-stand maneuvers in the anesthetized feline, we excited the hind limb musculature using intrafascicular multielectrode stimulation (IFMS) of the muscular branch of the sciatic nerve, the femoral nerve and the main branch of the sciatic nerve. Stimulation was achieved with either acutely or chronically implanted Utah Slanted Electrode Arrays (USEAs) via subsets of electrodes (1) that activated motor units in the extensor muscles of the hip, knee and ankle joints, (2) that were able to evoke large extension forces and (3) that manifested minimal coactivation of the targeted motor units. Three hind limb force-generation strategies were investigated, including sequential activation of independent motor units to increase force, and interleaved or simultaneous IFMS of three sets of six or more USEA electrodes that excited the hip, knee and ankle extensors. All force-generation strategies evoked stance, but the interleaved IFMS strategy also reduced muscle fatigue produced by repeated sit-to-stand maneuvers compared with fatigue produced by simultaneous activation of different motor neuron pools. These results demonstrate the use of interleaved IFMS as a means to recreate coordinated, fatigue-resistant multi-joint muscle forces in the unilateral hind limb. This muscle activation paradigm could provide a promising neuroprosthetic approach for the restoration of sit-to-stand transitions in individuals who are paralyzed by spinal cord injury, stroke or disease.

[1]  P. Carlson-Kuhta,et al.  Forms of forward quadrupedal locomotion. II. A comparison of posture, hindlimb kinematics, and motor patterns for upslope and level walking. , 1998, Journal of neurophysiology.

[2]  Reid R. Harrison,et al.  A Wireless Integrated Circuit for 100-Channel Charge-Balanced Neural Stimulation , 2009, IEEE Transactions on Biomedical Circuits and Systems.

[3]  R. Normann,et al.  Selective and Graded Recruitment of Cat Hamstring Muscles With Intrafascicular Stimulation , 2009, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[4]  Jon A. Mukand,et al.  Neuronal ensemble control of prosthetic devices by a human with tetraplegia , 2006, Nature.

[5]  D. Szarowski,et al.  Brain responses to micro-machined silicon devices , 2003, Brain Research.

[6]  P H Peckham,et al.  Tissue response to chronically stimulated implanted epimysial and intramuscular electrodes. , 1997, IEEE transactions on rehabilitation engineering : a publication of the IEEE Engineering in Medicine and Biology Society.

[7]  S. Salmons.  Adaptive change in electrically stimulated muscle: A framework for the design of clinical protocols , 2009, Muscle & nerve.

[8]  G. E. Goslow,et al.  The cat step cycle: Hind limb joint angles and muscle lengths during unrestrained locomotion , 1973, Journal of morphology.

[9]  T. Bajd,et al.  Electrical stimulation providing functional use of paraplegic patient muscles. , 1980, Medical progress through technology.

[10]  P. Manson,et al.  Biocompatibility of Fixation Materials in the Brain , 1997, Plastic and reconstructive surgery.

[11]  Richard A Normann,et al.  New functional electrical stimulation approaches to standing and walking , 2007, Journal of neural engineering.

[12]  R. Stein,et al.  Selective stimulation of cat sciatic nerve using an array of varying-length microelectrodes. , 2001, Journal of neurophysiology.

[13]  R A Normann,et al.  Multiple-Input Single-Output Closed-Loop Isometric Force Control Using Asynchronous Intrafascicular Multi-Electrode Stimulation , 2011, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[14]  David C. Martin,et al.  Neuronal cell loss accompanies the brain tissue response to chronically implanted silicon microelectrode arrays , 2005, Experimental Neurology.

[15]  Nathalie Crevier-Denoix,et al.  Strain and force transducers used in human and veterinary tendon and ligament biomechanical studies. , 2004, Clinical biomechanics.

[16]  G.A. Clark,et al.  Automated Stimulus-Response Mapping of High-Electrode-Count Neural Implants , 2009, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[17]  Patrick A Tresco,et al.  The brain tissue response to implanted silicon microelectrode arrays is increased when the device is tethered to the skull. , 2007, Journal of biomedical materials research. Part A.

[18]  R. Andersen,et al.  A floating metal microelectrode array for chronic implantation , 2007, Journal of Neuroscience Methods.

[19]  T. Yuen,et al.  Tissue response to potential neuroprosthetic materials implanted subdurally. , 1987, Biomaterials.

[20]  K. Yoshida,et al.  Selective stimulation of peripheral nerve fibers using dual intrafascicular electrodes , 1993, IEEE Transactions on Biomedical Engineering.

[21]  Huiru Zheng,et al.  Position-sensing technologies for movement analysis in stroke rehabilitation , 2005, Medical and Biological Engineering and Computing.

[22]  John P. Donoghue,et al.  Connecting cortex to machines: recent advances in brain interfaces , 2002, Nature Neuroscience.

[23]  A. Monster,et al.  Isometric force production by motor units of extensor digitorum communis muscle in man. , 1977, Journal of neurophysiology.

[24]  Warren M Grill,et al.  Implanted neural interfaces: biochallenges and engineered solutions. , 2009, Annual review of biomedical engineering.

[25]  R. Triolo,et al.  Preliminary performance of a surgically implanted neuroprosthesis for standing and transfers--where do we stand? , 2001, Journal of rehabilitation research and development.

[26]  A. Branner,et al.  A multielectrode array for intrafascicular recording and stimulation in sciatic nerve of cats , 2000, Brain Research Bulletin.

[27]  G A Clark,et al.  Non-invasive method for selection of electrodes and stimulus parameters for FES applications with intrafascicular arrays. , 2012, Journal of neural engineering.

[28]  J. Hoffer,et al.  Nerve cuffs for nerve repair and regeneration. , 2000, Progress in brain research.

[29]  M. Nicolelis,et al.  Reconstructing the Engram: Simultaneous, Multisite, Many Single Neuron Recordings , 1997, Neuron.

[30]  U Proske,et al.  Fatigue in mammalian skeletal muscle stimulated under computer control. , 2001, Journal of applied physiology.

[31]  Daniel McDonnall,et al.  Selective motor unit recruitment via intrafascicular multielectrode stimulation. , 2004, Canadian journal of physiology and pharmacology.

[32]  J L Smith,et al.  Forms of forward quadrupedal locomotion. I. A comparison of posture, hindlimb kinematics, and motor patterns for normal and crouched walking. , 1996, Journal of neurophysiology.

[33]  Suzanne S. Stensaas,et al.  Histopathological evaluation of materials implanted in the cerebral cortex , 1978, Acta Neuropathologica.

[34]  R. Normann,et al.  A method for pneumatically inserting an array of penetrating electrodes into cortical tissue , 2006, Annals of Biomedical Engineering.

[35]  T. Stieglitz,et al.  A transverse intrafascicular multichannel electrode (TIME) to interface with the peripheral nerve. , 2010, Biosensors & bioelectronics.

[36]  D. Durand,et al.  Functionally selective peripheral nerve stimulation with a flat interface nerve electrode , 2002, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[37]  Intraoperative Testing of Selectivity of Spiral Nerve Cuff Electrodes , 2005, Conference Proceedings. 2nd International IEEE EMBS Conference on Neural Engineering, 2005..

[38]  D. Graupe.  An overview of the state of the art of noninvasive FES for independent ambulation by thoracic level paraplegics , 2002, Neurological research.

[39]  Lisa Ness MacFadden.  Musculoskeletal modeling for intrafascicular multielectrode stimulation of the feline hindlimb , 2010 .

[40]  G E Loeb,et al.  Recruitment properties of intramuscular and nerve-trunk stimulating electrodes. , 2000, IEEE transactions on rehabilitation engineering : a publication of the IEEE Engineering in Medicine and Biology Society.

[41]  David C. Martin,et al.  Chronic neural recordings using silicon microelectrode arrays electrochemically deposited with a poly(3,4-ethylenedioxythiophene) (PEDOT) film , 2006, Journal of neural engineering.

[42]  Eduardo Fernández,et al.  Long-term stimulation and recording with a penetrating microelectrode array in cat sciatic nerve , 2004, IEEE Transactions on Biomedical Engineering.

[43]  Daryl R. Kipke,et al.  Voltage pulses change neural interface properties and improve unit recordings with chronically implanted microelectrodes , 2006, IEEE Transactions on Biomedical Engineering.

[44]  D. Marshall,et al.  Equine post-anesthetic lameness. A retrospective study. , 1990, Veterinary surgery : VS.

[45]  Bradley Greger,et al.  The functional consequences of chronic, physiologically effective intracortical microstimulation. , 2011, Progress in brain research.

[46]  Andrew B. Schwartz,et al.  Brain-Controlled Interfaces: Movement Restoration with Neural Prosthetics , 2006, Neuron.

[47]  K. Horch,et al.  Reduced fatigue in electrically stimulated muscle using dual channel intrafascicular electrodes with interleaved stimulation , 1993, Annals of Biomedical Engineering.

[48]  R. Normann,et al.  Interleaved, multisite electrical stimulation of cat sciatic nerve produces fatigue-resistant, ripple-free motor responses , 2004, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[49]  W.L.C. Rutten,et al.  Sensitivity and selectivity of intraneural stimulation using a silicon electrode array , 1991, IEEE Transactions on Biomedical Engineering.

[50]  T. Stieglitz,et al.  A biohybrid system to interface peripheral nerves after traumatic lesions: design of a high channel sieve electrode. , 2002, Biosensors & bioelectronics.

[51]  E. Maynard,et al.  A technique to prevent dural adhesions to chronically implanted microelectrode arrays , 2000, Journal of Neuroscience Methods.

[52]  P. Rack,et al.  The effects of length and stimulus rate on tension in the isometric cat soleus muscle , 1969, The Journal of physiology.