EMG Activation Patterns Associated with High Frequency, Long-Duration Intracortical Microstimulation of Primary Motor Cortex

Abstract

The delivery of high-frequency, long-duration intracortical microstimulation (HFLD-ICMS) to primary motor cortex (M1) in primates produces hand movements to a common final end-point regardless of the starting hand position (Graziano et al., 2002). We have confirmed this general conclusion. We further investigated the extent to which the (1) temporal pattern, (2) magnitude, and (3) latency of electromyographic (EMG) activation associated with HFLD-ICMS-evoked movements are dependent on task conditions, including limb posture. HFLD-ICMS was applied to layer V sites in M1 cortex. EMG activation with HFLD-ICMS was evaluated while two male rhesus macaques performed a number of tasks in which the starting position of the hand could be varied throughout the workspace. HFLD-ICMS-evoked EMG activity was largely stable across all parameters tested independent of starting hand position. The most common temporal pattern of HFLD-ICMS-evoked EMG activity (58% of responses) was a sharp rise to a plateau. The plateau level was maintained essentially constant for the entire duration of the stimulus train. The plateau pattern is qualitatively different from the largely bell-shaped patterns typical of EMG activity associated with natural goal directed movements (Brown and Cooke, 1990; Hoffman and Strick, 1999). HFLD-ICMS produces relatively fixed parameters of muscle activation independent of limb position. We conclude that joint movement associated with HFLD-ICMS occurs as a function of the length-tension properties of stimulus-activated muscles until an equilibrium between agonist and antagonist muscle force is achieved.

The Multiple Representations of Complex Digit Movements in Primary Motor Cortex Form the Building Blocks for Complex Grip Types in Capuchin Monkeys

“…More recently, LT-ICMS has been used to explore motor and parietal cortex in prosimians (Stepniewska et al, 2005(Stepniewska et al, , 2009(Stepniewska et al, , 2014, macaques (Griffin et al, 2014;Baldwin et al, 2018), and New World squirrel monkeys and owl monkeys (Gharbawie et al, 2010(Gharbawie et al, , 2011aStepniewska et al, 2014). Results from these studies were similar to those in the present investigation in that a gross topographic organization was observed in motor cortex.…”

“…Macaques have an opposable thumb and engage in a variety of dexterous manual behaviors using multiple types of precision grips (Macfarlane and Graziano, 2009). However, previous work that used LT-ICMS to explore motor cortex of macaques described hand movements in a different way (i.e., ICMS-evoked contraction pattern of hand muscles (Park et al, 2001;Overduin et al, 2012;Griffin et al, 2014) or did not provided details of precision-like grips at all (Graziano et al, 2002(Graziano et al, , 2005Gharbawie et al, 2011b). An exception was the study of Baldwin et al (2018), which described the fine details of digit movements evoked by LT-ICMS in motor and parietal cortex.…”

Revealing humans’ sensorimotor functions with electrical cortical stimulation

“…Notably, the true ethological nature of the complex synergies evoked through DES was recently questioned by Cheney and colleagues. In monkeys, these authors provided evidence that postural synergies evoked through cortical stimulation were not produced by natural patterns of EMG activity but instead resulted from an unnatural co-contraction of numerous 'hijacked' muscles that forced the limb to an equilibrium point [74,75]. However, the generality of these observations remains debatable for at least three reasons.…”

Muscle synergies obtained from comprehensive mapping of the primary motor cortex forelimb representation using high-frequency, long-duration ICMS

“…While stimulation results in a variety of movements to stable end points in space, some of these movements are natural looking, while others are not (Bonazzi et al 2013;Gharbawie et al 2011;Graziano et al 2005Graziano et al , 2002Harrison et al 2012;Ramanathan et al 2006;Van Acker et al 2014). HFLD-ICMS-evoked EMG also has a different timescale pattern compared with that of natural movement and has been found to be tonic or phasic-tonic 72% of the time (Griffin et al 2014). This time independence allowed one time bin (1,000 ms) to be used for the stimulus-evoked synergy calculations, while 100-ms time bins were used for voluntary synergies.…”

“…HFLD-ICMS was applied to a series of single M1 locations while the monkey performed the behavioral task. Stimulation typically interrupted the voluntary movement and caused the monkey's forelimb to move involuntarily (Griffin et al 2014). At the start of each data collection section, a manual hydraulic microdrive (FHC) coupled to a custom X-Y positioner was used to position a microelectrode at or near putative lamina V sites in M1 cortex.…”