Transcranial Magnetic Stimulation over Sensorimotor Cortex Disrupts Anticipatory Reflex Gain Modulation for Skilled Action

Abstract

Skilled interactions with new environments require flexible changes to the transformation from somatosensory signals to motor outputs. Transcortical reflex gains are known to be modulated according to task and environmental dynamics, but the mechanism of this modulation remains unclear. We examined reflex organization in the sensorimotor cortex. Subjects performed point-to-point arm movements into predictable force fields. When a small perturbation was applied just before the arm encountered the force field, reflex responses in the shoulder muscles changed according to the upcoming force field direction, indicating anticipatory reflex gain modulation. However, when a transcranial magnetic stimulation (TMS) was applied before the reflex response to such perturbations so that the silent period caused by TMS overlapped the reflex processing period, this modulation was abolished, while the reflex itself remained. Loss of reflex gain modulation could not be explained by reduced reflex amplitudes nor by peripheral effects of TMS on the muscles themselves. Instead, we suggest that TMS disrupted interneuronal networks in the sensorimotor cortex, which contribute to reflex gain modulation rather than reflex generation. We suggest that these networks normally provide the adaptability of rapid sensorimotor reflex responses by regulating reflex gains according to the current dynamical environment.

Goal-dependent modulation of the long-latency stretch response at the shoulder, elbow, and wrist

“…Briefly, the timing of the short-latency stretch response, appearing on the muscle ϳ25-50 ms after perturbation onset, requires that it engage a spinal circuit mediated by relatively large-diameter afferent fibers (PierrotDesilligny and Burke 2005). The neural basis of the longlatency stretch response is more complicated (for review see Pruszynski and Scott 2012), as it likely reflects the temporal overlap of several sources at multiple levels of the neuraxis, including spinal cord, brain stem, and cortex (Cheney and Fetz 1984;Evarts and Tanji 1976;Grey et al 2001;Kimura et al 2006;Kurtzer et al 2010Kurtzer et al , 2014Lourenço et al 2006;Matthews 1984;Matthews and Miles 1988;Omrani et al 2014;Pruszynski 2014;Pruszynski et al 2011a;Schuurmans et al 2009;Shemmell et al 2009). An added complication is that these distinct neural generators may have unique or overlapping functional capacity.…”

“…This position is supported by many demonstrations that muscular activity 50 -100 ms after a mechanical perturbation (i.e., the long-latency stretch response) shows a range of modulation that reflects voluntary motor control (for review see Pruszynski and Scott 2012;Shemmell et al 2010). Such modulation of the long-latency stretch response reflects sensitivity to task demands (Dietz et al 1994;Doemges andRack 1992a, 1992b;Hager-Ross et al 1996;Marsden et al 1981;Nashed et al 2012), movement decision-making processes (Nashed et al 2014;Selen et al 2012;Yang et al 2011), routing of sensory information across different muscles (Cole et al 1984;Dimitriou et al 2012;Marsden et al 1981;Mutha and Sainburg 2009;Ohki and Johansson 1999;Omrani et al 2013), as well as knowledge of the mechanical properties of the arm (Crevecoeur et al 2012;Crevecoeur and Scott 2013;Gielen et al 1988;Koshland et al 1991;Kurtzer et al 2008Kurtzer et al , 2009Kurtzer et al , 2013Kurtzer et al , 2014Pruszynski et al 2011a;Soechting and Lacquaniti 1988) and environment (Ahmadi-Pajouh et al 2012;Akazawa et al 1983;Bedingham and Tatton 1984;Cluff and Scott 2013;Dietz et al 1994;Kimura et al 2006;Krutky et al 2010;Perreault et al 2008;Pruszynski et al 2009;Shemmell et al 2009<...>…”

Respiratory, postural and spatio-kinetic motor stabilization, internal models, top-down timed motor coordination and expanded cerebello-cerebral circuitry: a review

“…"These findings indicate that, in addition to generating fast corrective response, the lumbar spinal cord generated some adjustments in hindlimb stepping patterns through experience" (Heng and de Leon, 2007, p. 8561). Such processes are also under descending cerebellar (van der Linden et al, 2007) and cerebral cortical (Kimura et al, 2006) control, and can even be modified voluntarily in humans after biofeedback training (Ludvig et al, 2007).…”

“…Controversy exists as to whether the models so acquired are stored in the cerebellum , or cerebral cortex areas such as the parietal area . The actual submovements so scheduled for task mastered motor skills might be directly controlled from the cerebral cortex (Heffner and Masterton, 1983;Kuyper, 1958;Liscic et al, 1998;Ludlow, 2005;Maertens de Noordhout et al, 1999;Teitti et al, 2008), or involve in a hierarchical manner of delegation, lower areas in the supraspinal nervous system, such as the cerebellum and other subcortical areas (van der Linden et al, 2007), and/or, processes lower down in the spinal cord (Kimura et al, 2006;van der Linden et al, 2007). Related this top-down control, the supraspinal adjustment of long-latency (45-100 ms) reflexes can also draw upon the cerebello-cerebral internal models of limb dynamics (Kurtzer et al, 2008).…”

“…Further, musculoskeletally more specific ones such as the reflexes that occur in other primates across the elbow are not found in humans (Illert and Kummel, 1999). Moreover, where reflexes occur, the human cerebral cortex can directly control their properties (Kimura et al, 2006). Indeed, humans can voluntarily learn to control them when trained with biofeedback (Ludvig et al, 2007), suggesting that humans have the capacity, if need be, to selectively limit their inappropriate involvement in movements.…”