A startling auditory stimulus (SAS) induces a reflex response involving, among other reactions, a strong contraction of the orbicularis oculi muscle (OOc) and subsequent eye closure. A SAS also induces the StartReact effect, a significant shortening of reaction time in subjects ready for task execution. We examined the obvious conflict appearing when a StartReact paradigm requires participants with eyes closed to open their eyes to look for a visual target. We recorded OOc EMG activity and eyelid movements in healthy volunteers who were instructed to open their eyes at perception of a somatosensory imperative stimulus (IS) and locate the position of a Libet's clock's hand shown on a computer screen at 80 cm distance. In 6 out of 20 trials, we delivered a SAS simultaneously with the IS. The main outcome measures were reaction time at onset of eyelid movement and the time gap (TG) separating subjective assessment of the clock's hand position from real IS issuing. Control experiments included reaction time to eye closing and target location with eyes open to the same IS. Reaction time was significantly faster in SAS than in noSAS trials and slower for eye opening than for eye closing in both conditions. In the eye-opening task, TG was significantly shorter in SAS with respect to noSAS trials, despite the presence of the SAS-related burst in the OOc before EMG cessation. Our results indicate that the StartReact effect speeds up eye opening and location of a target in the visual field despite the startle reaction opposing the task.

Complutense University of Madrid Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas Madrid Spain

Department of Neurology and Centre of Clinical Neuroscience 1st Medical Faculty Charles University Prague Czech Republic

Department of Neurology Hochzirl Hospital Zirl Austria

Department of Neurorehabilitation Hospital of Vipiteno Sterzing Vipiteno Sterzing Italy

Department of Radiology Rehabilitation and Physiotherapy School of Medicine National School of Occupational Medicine Carlos 3 Institute of Health Madrid Spain

EMG and Motor Control Unit Neurology Department Hospital Clínic University of Barcelona Barcelona Spain

Institut d'Investigacions Biomèdiques August Pi i Sunyer Hospital Clínic Barcelona Spain

Reasearch Unit for Neurorehabilitation of South Tyrol Bolzano Bozen Italy

Zobrazit více v PubMed

Alibiglou, L., & MacKinnon, C. D. (2012). The early release of planned movement by acoustic startle can be delayed by transcranial magnetic stimulation over the motor cortex. Journal of Physiology, 590(4), 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. Experimental Brain Research, 208(2), 237-243. https://doi.org/10.1007/s00221-010-2474-1

Aramideh, M., Ongerboer de Visser, B. W., Devriese, P. P., Bour, L. J., & Speelman, J. D. (1994). Electromyographic features of levator palpebrae superioris and orbicularis oculi muscles in blepharospasm. Brain, 117(1), 27-38. https://doi.org/10.1093/brain/117.1.27

Brown, P., Rothwell, J. C., Thompson, P. D., Britton, T. C., Day, B. L., & Marsden, C. D. (1991). New observations on the normal auditory startle reflex in man. Brain, 114(4), 1891-1902. https://doi.org/10.1093/brain/114.4.1891

Carlsen, A. N., Almeida, Q. J., & Franks, I. M. (2012). Startle decreases reaction time to active inhibition. Experimental Brain Research, 217(1), 7-14. https://doi.org/10.1007/s00221-011-2964-9

Carlsen, A. N., Chua, R., Inglis, J. T., Sanderson, D. J., & Franks, I. M. (2004). Can prepared responses be stored subcortically? Experimental Brain Research, 159(3), 301-309. https://doi.org/10.1007/s00221-004-1924-z

Carlsen, A. N., Chua, R., Inglis, J. T., Sanderson, D. J., & Franks, I. M. (2009). Differential effects of startle on reaction time for finger and arm movements. Journal of Neurophysiology, 101(1), 306-314. https://doi.org/10.1152/jn.00878.2007

Carlsen, A. N., & Maslovat, D. (2019). Startle and the StartReact effect: Physiological mechanisms. Journal of Clinical Neurophysiology, 36(6), 452-459. https://doi.org/10.1097/WNP.0000000000000582

Castellote, J. M., & Valls-Solé, J. (2015). The StartReact effect in tasks requiring end-point accuracy. Clinical Neurophysiology, 126(10), 1879-1885. https://doi.org/10.1016/j.clinph.2015.01.028

Castellote, J. M., & Valls-Solé, J. (2019). Temporal relationship between perceptual and physiological events triggered by nociceptive heat stimuli. Scientific Reports, 9(1), 3264. https://doi.org/10.1038/s41598-019-39509-3

Conrad, B., Benecke, R., & Goehmann, M. (1983). Premovement silent period in fast movement initiation. Experimental Brain Research, 51(2), 310-313. https://doi.org/10.1007/BF00237208

Correa, L. I., Cardenas, K., Casanova-Mollá, J., & Valls-Solé, J. (2019). Thermoalgesic stimuli induce prepulse inhibition of the blink reflex and affect conscious perception in healthy humans. Psychophysiology, 56(4), e13310. https://doi.org/10.1111/psyp.13310

Esteban, A., Traba, A., & Prieto, J. (2004). Eyelid movements in health and disease. The supranuclear impairment of the palpebral motility. Neurophysiologie Clinique/Clinical Neurophysiology, 34(1), 3-15. https://doi.org/10.1016/j.neucli.2004.01.002

Evinger, C., Manning, K. A., & Sibony, P. A. (1991). Eyelid movements. Mechanisms and normal data. Investigative Ophthalmology & Visual Science, 32(2), 387-400.

Gehricke, J. G., Ornitz, E. M., & Siddarth, P. (2002). Differentiating between reflex and spontaneous blinks using simultaneous recording of the orbicularis oculi electromyogram and the electro-oculogram in startle research. International Journal of Psychophysiology, 44(3), 261-268. https://doi.org/10.1016/s0167-8760(02)00008-9

Haith, A. M., Pakpoor, J., & Krakauer, J. W. (2016). Independence of movement preparation and movement initiation. Journal of Neuroscience, 36(10), 3007-3015. https://doi.org/10.1523/JNEUROSCI.3245-15.2016

Honeycutt, C. F., Kharouta, M., & Perreault, E. J. (2013). Evidence for reticulospinal contributions to coordinated finger movements in humans. Journal of Neurophysiology, 110(7), 1476-1483. https://doi.org/10.1152/jn.00866.2012

Honeycutt, C. F., Tresch, U. A., & Perreault, E. J. (2015). Startling acoustic stimuli can evoke fast hand extension movements in stroke survivors. Clinical Neurophysiology, 126(1), 160-164. https://doi.org/10.1016/j.clinph.2014.05.025

Kofler, M., Müller, J., Reggiani, L., & Valls-Solé, J. (2001a). Influence of gender on auditory startle responses. Brain Research, 921(1-2), 206-210. https://doi.org/10.1016/s0006-8993(01)03120-1

Kofler, M., Müller, J., Reggiani, L., & Valls-Solé, J. (2001b). Influence of age on auditory startle responses in humans. Neuroscience Letters, 307(2), 65-68. https://doi.org/10.1016/s0304-3940(01)01908-5

Kumru, H., & Valls-Solé, J. (2006). Excitability of the pathways mediating the startle reaction before execution of a voluntary movement. Experimental Brain Research, 169(3), 427-432. https://doi.org/10.1007/s00221-005-0156-1

Leote, J., Castellote, J. M., Casanova-Molla, J., Navarro-Otano, J., Nunes, R. G., Ferreira, H. A., & Valls-Solé, J. (2018). Motor preparation in picture naming tasks. Brain and Language, 180-182, 24-30. https://doi.org/10.1016/j.bandl.2018.04.002

Leow, L. A., Uchida, A., Egberts, J. L., Riek, S., Lipp, O. V., Tresilian, J., & Marinovic, W. (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

Libet, B. (2004). Mind time. Harvard University Press.

Libet, B., Gleason, C. A., Wright, E. W., & Pearl, D. K. (1983). Time of conscious intention to act in relation to onset of cerebral activity (readiness-potential). Brain, 106(3), 623-642. https://doi.org/10.1093/brain/106.3.623

Marinovic, W., Milford, M., Carroll, T., & Riek, S. (2015). The facilitation of motor actions by acoustic and electric stimulation. Psychophysiology, 52(12), 1698-1710. https://doi.org/10.1111/psyp.12540

Maslovat, D., Hodges, N. J., Chua, R., & Franks, I. M. (2011). Motor preparation of spatially and temporally defined movements: Evidence from startle. Journal of Neurophysiology, 106(2), 885-894. https://doi.org/10.1152/jn.00166.2011

Maslovat, D., Kennedy, P. M., Forgaard, C. J., Chua, R., & Franks, I. M. (2012). The effects of prepulse inhibition timing on the startle reflex and reaction time. Neuroscience Letters, 513(2), 243-247. https://doi.org/10.1016/j.neulet.2012.02.052

Nardone, A., & Schieppati, M. (1988). Postural adjustments associated with voluntary contraction of leg muscles in standing man. Experimental Brain Research, 69(3), 469-480. https://doi.org/10.1007/BF00247301

Nonnekes, J., de Kam, D., Oude Nijhuis, L. B., van Geel, K., Bloem, B. R., Geurts, A., & Weerdesteyn, V. (2015). StartReact effects support different pathophysiological mechanisms underlying freezing of gait and postural instability in Parkinson's disease. PLoS One, 10(3), e0122064. https://doi.org/10.1371/journal.pone.0122064

Nonnekes, J., Oude Nijhuis, L. B., de Niet, M., de Bot, S. T., Pasman, J. W., van de Warrenburg, B. P. C., Bloem, B. R., Weerdesteyn, V., & Geurts, A. C. (2014). StartReact restores reaction time in HSP: Evidence for subcortical release of a motor program. Journal of Neuroscience, 34(1), 275-281. https://doi.org/10.1523/JNEUROSCI.2948-13.2014

Queralt, A., Valls-Solé, J., & Castellote, J. M. (2010). Speeding up gait initiation and gait-pattern with a startling stimulus. Gait and Posture, 31(2), 185-190. https://doi.org/10.1016/j.gaitpost.2009.10.003

Queralt, A., Weerdesteyn, V., van Duijnhoven, H. J., Castellote, J. M., Valls-Solé, J., & Duysens, J. (2008). The effects of an auditory startle on obstacle avoidance during walking. Journal of Physiology, 586(18), 4453-4463. https://doi.org/10.1113/jphysiol.2008.156042

Reynolds, R. F., & Day, B. L. (2007). Fast visuomotor processing made faster by sound. Journal of Physiology, 583(3), 1107-1115. https://doi.org/10.1113/jphysiol.2007.136192

Sanegre, M. T., Castellote, J. M., Haggard, P., & Valls-Solé, J. (2004). The effects of a startle on awareness of action. Experimental Brain Research, 155(4), 527-531. https://doi.org/10.1007/s00221-004-1849-6

Serranová, T., Jech, R., Martí, M. J., Modreanu, R., Valldeoriola, F., Sieger, T., Růžička, E., & Valls-Solé, J. (2012). A loud auditory stimulus overcomes voluntary movement limitation in cervical dystonia. PLoS One, 7(10), e46586. https://doi.org/10.1371/journal.pone.0046586

Siegmund, G. P., Inglis, J. T., & Sanderson, D. J. (2001). Startle response of human neck muscles sculpted by readiness to perform ballistic head movements. Journal of Physiology, 535(1), 289-300. https://doi.org/10.1111/j.1469-7793.2001.00289.x

Smith, V., Maslovat, D., & Carlsen, A. N. (2019). StartReact effects are dependent on engagement of startle reflex circuits: Support for a subcortically mediated initiation pathway. Journal of Neurophysiology, 122(6), 2541-2547. https://doi.org/10.1152/jn.00505.2019

Stevenson, A. J., Chiu, C., Maslovat, D., Chua, R., Gick, B., Blouin, J. S., & Franks, I. M. (2014). Cortical involvement in the StartReact effect. Neuroscience, 269, 21-34. https://doi.org/10.1016/j.neuroscience.2014.03.041

Sutter, K., Nonnekes, J., Dibilio, V., Geurts, A. C., & Weerdesteyn, V. (2016). Does the StartReact effect apply to first-trial reactive movements? PLoS One, 11(4), e0153129. https://doi.org/10.1371/journal.pone.0153129

Terao, Y., Fukuda, H., Sugiyama, Y., Inomata-Terada, S., Tokushige, S. I., Hamada, M., & Ugawa, Y. (2018). Recording horizontal saccade performances accurately in neurological patients using electro-oculogram. Journal of Visualized Experiments, 133, 56934. https://doi.org/10.3791/56934

Valls-Solé, J. (2004). Contribution of subcortical motor pathways to the execution of ballistic movements. Supplement Clinical Neurophysiology, 57, 554-562. https://doi.org/10.1016/s1567-424x(09)70394-0

Valls-Solé, J., Kofler, M., Kumru, H., Castellote, J. M., & Sanegre, M. T. (2005). Startle-induced reaction time shortening is not modified by prepulse inhibition. Experimental Brain Research, 165(4), 541-548. https://doi.org/10.1007/s00221-005-2332-8

Valls-Solé, J., Rothwell, J. C., Goulart, F., Cossu, G., & Munoz, E. (1999). Patterned ballistic movements triggered by a startle in healthy humans. Journal of Physiology, 516(3), 931-938. https://doi.org/10.1111/j.1469-7793.1999.0931u.x

Valls-Solé, J., Valldeoriola, F., Molinuevo, J. L., Cossu, G., & Nobbe, F. (1999). Prepulse modulation of the startle reaction and the blink reflex in normal human subjects. Experimental Brain Research, 129(1), 49-56. https://doi.org/10.1007/s002210050935