Analysis of the Effectiveness of Sub-sensory Electrical Noise Stimulation During Visuomotor Adaptations in Different Visual Feedback Conditions

Sub-sensory electrical noise stimulation has been shown to improve motor performance in tasks that mainly rely on proprioceptive feedback. During the execution of movements such as reaching, proprioceptive feedback combines dynamically with visual feedback. It is still unclear whether boosting proprioceptive information in tasks where proprioception mixes with vision can influence motor performance. To better understand this point, we tested the effect of electrical noise stimulation applied superficially to the muscle spindles during four different experiments consisting of isometric reaching tasks under different visual feedback conditions. The first experiment (n = 40) consisted of a reach-and-hold task where subjects had to hold a cursor on a target for 30 s and had visual feedback removed 10 s into the task. Subjects performed 30 repetitions of this task with different stimulation levels, including no stimulation. We observed that trials in which the stimulation was present displayed smaller movement variability. Moreover, we observed a positive correlation between the level of stimulation and task performance. The other three experiments consisted of three versions of an isometric visuomotor adaptation task where subjects were asked to reach to random targets in <1.5 s (otherwise incurring in negative feedback) while overcoming a 45° clockwise rotation in the mapping between the force exerted and the movement of the cursor. The three experiments differed in the visual feedback presented to the subjects, with one group (n = 20) performing the experiment with full visual feedback, one (n = 10) with visual feedback restricted only to the beginning of the trajectory, and one (n = 10) without visual feedback of the trajectory. All subjects performed their experiment twice, with and without stimulation. We did not observe substantial effects of the stimulation when visual feedback was present (either completely or partially). We observed a limited effect of the stimulation in the absence of visual feedback consisting in a significant smaller number of negative-feedback trials and a significant smaller movement time in the first block of the adaptation phase. Our results suggest that sub-sensory stimulation can be beneficial when proprioception is the main feedback modality but mostly ineffective in tasks where visual feedback is actively employed.

[1]  Philip N. Sabes,et al.  Multisensory Integration during Motor Planning , 2003, The Journal of Neuroscience.

[2]  Daniel M Wolpert,et al.  Role of uncertainty in sensorimotor control. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[3]  J. Collins,et al.  Noise-enhanced human sensorimotor function , 2003, IEEE Engineering in Medicine and Biology Magazine.

[4]  Silvia Conforto,et al.  Consistent visuomotor adaptations and generalizations can be achieved through different rotations of robust motor modules , 2018, Scientific Reports.

[5]  André Fabio Kohn,et al.  Effectiveness of electrical noise in reducing postural sway: a comparison between imperceptible stimulation applied to the anterior and to the posterior leg muscles , 2014, European Journal of Applied Physiology.

[6]  Scott E. Ross,et al.  Effect of Coordination Training With and Without Stochastic Resonance Stimulation on Dynamic Postural Stability of Subjects With Functional Ankle Instability and Subjects With Stable Ankles , 2006, Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine.

[7]  John W. Krakauer,et al.  Independent learning of internal models for kinematic and dynamic control of reaching , 1999, Nature Neuroscience.

[8]  Britne A. Shabbott,et al.  Learning a visuomotor rotation: simultaneous visual and proprioceptive information is crucial for visuomotor remapping , 2010, Experimental Brain Research.

[9]  L. Gammaitoni,et al.  Stochastic resonance and the dithering effect in threshold physical systems. , 1995, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[10]  Kelsey Petersen,et al.  Sensory enhancing insoles improve athletic performance during a hexagonal agility task. , 2016, Journal of biomechanics.

[11]  Ferdinando A Mussa-Ivaldi,et al.  Interaction of visual and proprioceptive feedback during adaptation of human reaching movements. , 2005, Journal of neurophysiology.

[12]  Carson C. Chow,et al.  Aperiodic stochastic resonance in excitable systems. , 1995, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[13]  Paolo Bonato,et al.  Noise‐enhanced balance control in patients with diabetes and patients with stroke , 2006, Annals of neurology.

[14]  André Fabio Kohn,et al.  Imperceptible electrical noise attenuates isometric plantar flexion force fluctuations with correlated reductions in postural sway , 2011, Experimental Brain Research.

[15]  O. Arias-Carrión,et al.  Effect of mechanical tactile noise on amplitude of visual evoked potentials: multisensory stochastic resonance. , 2015, Journal of neurophysiology.

[16]  B. Edin,et al.  Muscle afferent responses to isometric contractions and relaxations in humans. , 1990, Journal of neurophysiology.

[17]  E. A. Fleishman,et al.  Role of kinesthetic and spatialvisual abilities in perceptual-motor learning. , 1963, Journal of experimental psychology.

[18]  Borís Burle,et al.  Direct evidence for cortical suppression of somatosensory afferents during visuomotor adaptation. , 2009, Cerebral cortex.

[19]  John W Krakauer,et al.  Motor learning and consolidation: the case of visuomotor rotation. , 2009, Advances in experimental medicine and biology.

[20]  Frank Huethe,et al.  Improved Sensorimotor Performance via Stochastic Resonance , 2012, The Journal of Neuroscience.

[21]  J. Collins,et al.  Noise-enhanced balance control in older adults , 2002, Neuroreport.

[22]  P. Weinhold,et al.  A kinetic and kinematic analysis of the effect of stochastic resonance electrical stimulation and knee sleeve during gait in osteoarthritis of the knee. , 2014, Journal of applied biomechanics.

[23]  S. Schaal.  The Computational Neurobiology of Reaching and Pointing — A Foundation for Motor Learning by Reza Shadmehr and Steven P. Wise , 2007 .

[24]  Philip N. Sabes,et al.  Flexible strategies for sensory integration during motor planning , 2005, Nature Neuroscience.

[25]  Lara A Boyd,et al.  Preserved motor learning after stroke is related to the degree of proprioceptive deficit , 2009, Behavioral and Brain Functions.

[26]  B T Bates,et al.  Single-subject methodology: an alternative approach. , 1996, Medicine and science in sports and exercise.

[27]  N Teasdale,et al.  Mirror drawing in a deafferented patient and normal subjects , 1992, Neurology.

[28]  Frank Moss,et al.  Noise in human muscle spindles , 1996, Nature.

[29]  Kelvin E. Jones,et al.  Proprioceptive feedback is reduced during adaptation to a visuomotor transformation: preliminary findings , 2001, Neuroreport.

[30]  E. Delahunt,et al.  Effect of noise stimulation below and above sensory threshold on postural sway during a mildly challenging balance task. , 2018, Gait & posture.

[31]  Attila Priplata,et al.  Noise-enhanced human balance control. , 2002, Physical review letters.

[32]  A. Villringer,et al.  Electrical noise modulates perception of electrical pulses in humans: sensation enhancement via stochastic resonance. , 2014, Journal of neurophysiology.

[33]  Reza Shadmehr,et al.  Distinct neural circuits for control of movement vs. holding still. , 2017, Journal of neurophysiology.