Abstract
StartReact elicits faster, larger, and more appropriate muscle activation in stroke survivors but has been only cursorily studied to date during multi-jointed reaching. Our objective was to evaluate StartReact on unrestricted, two-dimensional point-to-point reaching tasks post-stroke. Data from 23 individuals with stroke were collected during point-to-point reaching. Voluntary and StartReact trials were compared between mild, severe/moderate, and the unimpaired arm. StartReact showed an increase in probability of muscle activity, larger muscle activity amplitude, and faster muscle activity onset. Despite changes in muscle activity, metrics of movement (distance, final error, linear deviation) were not different between StartReact and Voluntary trials except in severe/moderate stroke who had larger reaching distances during StartReact. While StartReact impacted many metrics of muscle activity, the most profound effect was on the probability of muscle activity increasing 34% compared to voluntary which allowed severe/moderate subjects to increase reaching distance but did not translate to decrease in final error suggesting that the additional movement was not always directed towards the appropriate target. These results indicate that SR has the capacity to activate paralyzed muscle in severe/moderate patients, but future studies are needed to explore the possible use of SR in the rehabilitation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alibiglou L, MacKinnon CD (2012) The early release of planned movement by acoustic startle can be delayed by transcranial magnetic stimulation over the motor cortex. J Physiol 590:919–936. https://doi.org/10.1113/jphysiol.2011.219592
Anzak A, Tan H, Pogosyan A, Brown P (2011) Doing better than your best: loud auditory stimulation yields improvements in maximal voluntary force. Exp Brain Res 208:237–243. https://doi.org/10.1007/s00221-010-2474-1
Bagesteiro LB, Sainburg RL (2003) Nondominant arm advantages in load compensation during rapid elbow joint movements. J Neurophysiol 90:1503–1513. https://doi.org/10.1152/jn.00189.2003
Baker SN, Perez MA (2017) Reticulospinal contributions to gross hand function after human spinal cord injury. J Neurosci 37:9778–9784. https://doi.org/10.1523/JNEUROSCI.3368-16.2017
Bates D (2005) Fitting linear mixed models in R. R News 51:27–30
Carlsen AN, Chua R, Inglis JT et al (2003) Startle response is dishabituated during a reaction time task. Exp Brain Res 152:510–518. https://doi.org/10.1007/s00221-003-1575-5
Carlsen AN, Maslovat D, Lam MY et al (2011) Considerations for the use of a startling acoustic stimulus in studies of motor preparation in humans. Neurosci Biobehav Rev 35:366–376. https://doi.org/10.1016/J.NEUBIOREV.2010.04.009
Carlsen AN, Almeida QJ, Franks IM (2012) Startle decreases reaction time to active inhibition. Exp Brain Res 217:7–14. https://doi.org/10.1007/s00221-011-2964-9
Carlsen AN, Almeida QJ, Franks IM (2013) Using a startling acoustic stimulus to investigate underlying mechanisms of bradykinesia in Parkinson’s disease. Neuropsychologia 51:392–399. https://doi.org/10.1016/J.NEUROPSYCHOLOGIA.2012.11.024
Castellote JM, Kofler M (2018) StartReact effects in first dorsal interosseous muscle are absent in a pinch task, but present when combined with elbow flexion. PLoS ONE. https://doi.org/10.1371/journal.pone.0201301
Castellote JM, Valls-Solé J (2015) The StartReact effect in tasks requiring end-point accuracy. Clin Neurophysiol 126:1879–1885. https://doi.org/10.1016/J.CLINPH.2015.01.028
Choudhury S, Shobhana A, Singh R et al (2019) The Relationship between enhanced reticulospinal outflow and upper limb function in chronic stroke patients. Neurorehabil Neural Repair. https://doi.org/10.1177/1545968319836233
Coppens MJM, Roelofs JMB, Donkers NAJ et al (2018) A startling acoustic stimulus facilitates voluntary lower extremity movements and automatic postural responses in people with chronic stroke. J Neurol 265:1625–1635. https://doi.org/10.1007/s00415-018-8889-5
Cressman EK, Carlsen AN, Chua R, Franks IM (2006) Temporal uncertainty does not affect response latencies of movements produced during startle reactions. Exp Brain Res 171:278–282. https://doi.org/10.1007/s00221-006-0459-x
Hogan N, Sudbury KHI et al (1994) Interactive robotic therapist. Massachusetts Institute of Technology, Cambridge
Honeycutt CF, Perreault EJ (2012) Planning of ballistic movement following stroke: insights from the startle reflex. PLoS ONE 7:e43097. https://doi.org/10.1371/journal.pone.0043097
Honeycutt CF, Perreault EJ (2014) Deficits in startle-evoked arm movements increase with impairment following stroke. Clin Neurophysiol 125:1682–1688. https://doi.org/10.1016/j.clinph.2013.12.102
Honeycutt CF, Tresch UA, Perreault EJ (2015) Startling acoustic stimuli can evoke fast hand extension movements in stroke survivors. Clin Neurophysiol 126:160–164. https://doi.org/10.1016/j.clinph.2014.05.025
Jankelowitz SK, Colebatch JG (2004) The acoustic startle reflex in ischemic stroke. Neurology 62:114–116. https://doi.org/10.1212/01.WNL.0000101711.48946.35
Kirkpatrick NJ, Ravichandran VJ, Perreault EJ et al (2018) Evidence for startle as a measurable behavioral indicator of motor learning. PLoS ONE 13:e0195689. https://doi.org/10.1371/journal.pone.0195689
Leow L-A, Uchida A, Egberts J-L et al (2018) Triggering mechanisms for motor actions: the effects of expectation on reaction times to intense acoustic stimuli. Neuroscience 393:226–235. https://doi.org/10.1016/j.neuroscience.2018.10.008
Marinovic W, Brauer SG, Hayward KS et al (2016) Electric and acoustic stimulation during movement preparation can facilitate movement execution in healthy participants and stroke survivors. Neurosci Lett 618:134–138. https://doi.org/10.1016/J.NEULET.2016.03.009
Marinovic W, Tresilian J, Chapple JL et al (2017) Unexpected acoustic stimulation during action preparation reveals gradual re-specification of movement direction. Neuroscience 348:23–32. https://doi.org/10.1016/j.neuroscience.2017.02.016
Maslovat D, Carlsen AN, Chua R, Franks IM (2009) Response preparation changes during practice of an asynchronous bimanual movement. Exp Brain Res 195:383–392. https://doi.org/10.1007/s00221-009-1801-x
Maslovat D, Hodges NJ, Chua R, Franks IM (2011) Motor preparation of spatially and temporally defined movements: evidence from startle. J Neurophysiol 125:226–240. https://doi.org/10.1037/a0022567
Nonnekes J, Geurts ACH, Oude Nijhuis LB et al (2014a) Reduced StartReact effect and freezing of gait in Parkinson’s disease: two of a kind? J Neurol 261:943–950. https://doi.org/10.1007/s00415-014-7304-0
Nonnekes J, Nijhuis LBO, de Niet M et al (2014b) StartReact restores reaction time in HSP: evidence for subcortical release of a motor program. J Neurosci 34:275–281. https://doi.org/10.1523/JNEUROSCI.2948-13.2014
Ossanna MR, Zong X, Ravichandran VJ, Honeycutt CF (2019) Startle evokes nearly identical movements in multi-jointed, two-dimensional reaching tasks. Exp Brain Res 237:71–80. https://doi.org/10.1007/s00221-018-5399-8
Pinheiro JC, Bates D (2000) Linear mixed-effects models: basic concepts and examples. In: Mixed-effects models in S and S-PLUS. Springer, New York, pp 3–56. https://doi.org/10.1007/0-387-22747-4_1
Ravichandran VJ, Honeycutt CF, Shemmell J, Perreault EJ (2013) Instruction-dependent modulation of the long-latency stretch reflex is associated with indicators of startle. Exp brain Res 230:59–69. https://doi.org/10.1007/s00221-013-3630-1
Sabut SK, Sikdar C, Kumar R, Mahadevappa M (2011) Functional electrical stimulation of dorsiflexor muscle: effects on dorsiflexor strength, plantarflexor spasticity, and motor recovery in stroke patients. NeuroRehabilitation 29:393–400. https://doi.org/10.3233/NRE-2011-0717
Sainburg RL, Poizner H, Ghez C (1993) Loss of proprioception produces deficits in interjoint coordination. J Neurophysiol 70:2136–2147. https://doi.org/10.1152/jn.1993.70.5.2136
Schaefer SY, Haaland KY, Sainburg RL (2009) Dissociation of initial trajectory and final position errors during visuomotor adaptation following unilateral stroke. Brain Res 1298:78–91. https://doi.org/10.1016/j.brainres.2009.08.063
Siegmund GP, Inglis JT, Sanderson DJ (2001) Startle response of human neck muscles sculpted by readiness to perform ballistic head movements. J Physiol 535:289–300
Sutter K, Nonnekes J, Dibilio V et al (2016) Does the StartReact effect apply to first-trial reactive movements? PLoS ONE. https://doi.org/10.1371/journal.pone.0153129
Tazoe T, Perez MA (2017) Cortical and reticular contributions to human precision and power grip. J Physiol 595:2715–2730. https://doi.org/10.1113/JP273679
Valls-Solé J, Rothwell JC, Goulart F et al (1999) Patterned ballistic movements triggered by a startle in healthy humans. J Physiol 516:931–938. https://doi.org/10.1111/j.1469-7793.1999.0931u.x
van Lith BJH, Coppens MJM, Nonnekes J et al (2018) StartReact during gait initiation reveals differential control of muscle activation and inhibition in patients with corticospinal degeneration. J Neurol 265:2531–2539. https://doi.org/10.1007/s00415-018-9027-0
Wright ZA, Carlsen AN, MacKinnon CD, Patton JL (2015) Degraded expression of learned feedforward control in movements released by startle. Exp Brain Res 233:2291–2300. https://doi.org/10.1007/s00221-015-4298-5
Acknowledgements
This study was made possible through funding from the National Institutes of Health (R00 HD073240). Many thanks to members of the Human Mobility Lab for the guidance, assistance, and support throughout this research study.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by John Rothwell.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Rahimi, M., Honeycutt, C.F. StartReact increases the probability of muscle activity and distance in severe/moderate stroke survivors during two-dimensional reaching task. Exp Brain Res 238, 1219–1227 (2020). https://doi.org/10.1007/s00221-020-05797-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-020-05797-9