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

Abstract

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 bi-articular. 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.

Intrafascicular stimulation of monkey arm nerves evokes coordinated grasp and sensory responses

“…Currents to evoke these contractions were not directly measured (given the use of constant-voltage stimulation at 3 V) but lie below levels that could damage tissue with short-term stimulation sessions, between 5 and 50 A, as documented in the cat, including for short-term stimulation across multiple sessions (Branner et al 2004;Frankel et al 2011;Normann et al 2012). …”

“…So long as stimulation through the USEA electrodes can evoke responses in independent, nonoverlapping motor units, the same approach may work for monkey arm nerves, and presumably for human nerves as well. However, the time constraints of the present acute studies precluded systematic investigations of the overlap of USEA electrode responses and the effects of interleaved stimulation on fatigue resistance (see Normann et al 2012 for details of the overlap and fatigability tests).…”

“…Although all neural implants face the problems associated with tissue response, central nervous system (CNS) implants of UEAs are subjected to less motion than nerve implants, and traditionally have been more reliable (Simeral et al 2011) than long-term USEA implants in initial studies (Branner et al 2004). However, recent and ongoing research has demonstrated substantive improvements in both long-term recording and stimulating capabilities of USEAs in cat sciatic nerve Frankel et al 2011;Ledbetter et al 2011;Normann et al 2012), which may translate to comparable success for USEAs in monkey arm nerves, and ultimately for clinical applications.…”

“…Thus intrafascicular nerve stimulation with USEAs may also provide an improved level of hand movements, compared with conventional FES. Among other advantages, a USEA may access multiple muscles with a single implant site and independent access to multiple different motor units within the same muscle, thereby also allowing more graded force control and more fatigue-resistant movements via interleaved stimulation (Normann et al 2012). It may also allow access to intrinsic hand muscles, which is difficult to achieve with conventional extraneural nerve stimulation.…”

Brain-controlled muscle stimulation for the restoration of motor function

“…Implanting large numbers of intramuscular electrodes is effective, but requires extensive surgery. Multi-contact peripheral nerve stimulation is being investigated as a means to provide access to a large numbers of muscles with fewer implant sites (Badia et al, 2011; Brill et al, 2009; Normann et al, 2012; Rodriguez et al, 2000; Schiefer et al, 2010; Tyler et al, 2002). All of these methods induce greater than normal fatigue, because of their inability to reproduce normal motor unit recruitment order.…”