Abstract
The startle reaction (SR) is usually understood as an involuntary reaction to an unexpected sensory input. However, there is evidence that the mechanisms involved in the SR contribute also to the execution of actions that we consider voluntary. We need to exert a fine control of the motor output, which usually involves inhibition of the reflex reaction but it may also imply letting the SR manifest, shaped in accordance with our willed actions. The latter occurs mainly with relatively simple ballistic movements but it has also been shown to occur in complex movements. In this review, we describe arguments published in the literature in favour of the contribution of subcortical motor tracts involved in the generation of the SR to the execution of voluntary movements. Some of these studies have brought insight on the mechanisms accounting for motor preparation and execution of voluntary movements.
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References
Bisdorff AR, Bronstein AM, Gresty MA (1994) Responses in neck and facial muscles to sudden free fall and a startling auditory stimulus. Electroenceph clin Neurophysiol 93:409–416
Blumenthal TD, Gescheider GA (1987) Modification of the acoustic startle reflex by a tactile prepulse: the effects of stimulus onset asynchrony and prepulse intensity. Psychophysiology 24:320–327
Blumenthal TD, Cuthbert BN, Filion DL, Hackley S, Lipp OV, Van Boxtel A (2005) Committee report: guidelines for human startle eyeblink electromyographic studies. Psychophysiology 42:1–15
Boelhouwer AJW, Teurlings RJMA, Brunia CHM (1991) The effect of an acoustic warning stimulus upon the electrically elicited blink reflex in humans. Psychophysiology 28:133–139
Boulu Ph, Willer JC, Cambier J (1981) Analyse electrophysiologique du réflexe de clignement chez l’homme: interaction des afferences sensitives segmentaires et intersegmentaires, des afferences auditives et visuelles. Rev Neurol 137:523–533
Brown P, Rothwell JC, Thompson PD, Britton TC, Day BL, Marsden CD (1991a) New observations on the normal auditory startle reflex in man. Brain 11:1891–1902
Brown P, Day BL, Rothwell JC, Thompson PD, Marsden CD (1991b) The effect of posture on the normal and pathological auditory startle reflex. J Neurol Neurosurg Psychiatry 54:892–897
Buford JA, Davidson AG (2004) Movement-related and preparatory activity in the reticulospinal system of the monkey. Exp Brain Res 159:284–300
Carlsen AN, Chua R, Inglis JT, Sanderson DJ, Franks IM (2003) Startle response is dishabituated during a reaction time task. Exp Brain Res 152:510–518
Carlsen AN, Chua R, Inglis JT, Sanderson DJ, Franks IM (2004a) Can prepared responses be stored subcortically? Exp Brain Res 159:301–309
Carlsen AN, Chua R, Inglis JT, Sanderson DJ, Franks IM (2004b) Prepared movements are elicited early by startle. J Mot Behav 36:253–264
Carlsen AN, Dakin CJ, Chua R, Franks IM (2007) Startle produces early response latencies that are distinct from stimulus intensity effects. Exp Brain Res 176:199–205
Castellote JM, Kumru H, Queralt A, Valls-Sole J (2007) A startle speeds up the execution of externally guided saccades. Exp Brain Res 177:129–136
Chabot CC, Taylor DH (1992) Circadian modulation of the rat acoustic startle response. Behav Neurosci 106:846–852
Chokroverty S, Walczak T, Hening W (1992) Human startle reflex: technique and criteria for abnormal response. Electroenceph clin Neurophysiol 85:236–242
Costa J, Valls-Sole J, Valldeoriola F, Pech C, Rumia J (2006) Single subthalamic nucleus deep brain stimuli inhibit the blink reflex in Parkinson’s disease patients. Brain 129:1758–1767
Davis M, Gendelman PM (1977) Plasticity of the acoustic startle response in the acutely decerebrate rat. J Comp Physiol Psychol 91:549–563
Davis M, Gendelman DS, Tischler MD, Gendelman PM (1982) A primary acoustic startle circuit: lesion and stimulation studies. J Neurosci 2:791–805
Davis M (1996) Differential roles of the amygdala and bed nucleus of the stria terminalis in conditioned fear and startle enhanced by corticotropin-releasing hormone. In: Ono T, McNaughton BL, Molotchnikoff S, Rolls ET, Nishijo H (eds) Perception memory and emotion. Elsevier Ltd, Oxford, pp 525–548
Delwaide PJ, Schepens B (1995) Auditory startle (audio-spinal) reaction in normal man: EMG responses and H reflex changes in antagonistic lower limb muscles. Electroenceph clin Neurophysiol 97:416–423
Dimberg U (1990) Facial electromyographic reactions and autonomic activity to auditory stimuli. Biol Psychol 31:137–147
Eimer M (1998) The lateralized readiness potential as an on-line measure of selective response activation. Behav Res Methods Instrum Comput 30:146–156
Fendt M, Koch M (1999) Cholinergic modulation of the acoustic startle response in the caudal pontine reticular nucleus of the rat. Eur J Pharmacol 370:101–107
Fisher RJ, Sharott A, Kühn AA, Brown P (2004) Effects of combined cortical and acoustic stimuli on muscle activity. Exp Brain Res 157:1–9
Floeter MK, Rothwell JC (1999) Releasing the brakes before pressing the gas pedal. Neurology 53:664–665
Furubayashi T, Ugawa Y, Terao Y, Hanajima R, Sakai K, Machii K, Mochizuki H, Shiio Y, Uesugi H, Enomoto H, Kanazawa I (2000) The human hand motor area is transiently suppressed by an unexpected acoustic stimulus. Clin Neurophysiol 111:178–183
Gautier CH, Cook EW (1997) Relationship between startle and cardiovascular reactivity Psychophysiology 34:87–96
Gielen SC, Schmidt RA, Van den Heuvel PJ (1983) On the nature of intersensory facilitation of reaction time. Percept Psychophys 34:161–168
Gogan P (1970) The startle and orienting reactions in man. A study of their characteristics and habituation. Brain Research 18:117–135
Gokin AP, Karpukhina MV (1985) Reticular structures in the cat brain involved in startle to somatic stimuli of various modalities. Neurophysiology 17:278–286
Graham FK (1975) The more or less startling effects of weak prestimulation. Psychophysiology 12:238–248
Grillon C, Ameli R, Wood SW, Merikangas K, Davis M (1991) Fear-potentiated startle in humans: effects of anticipatory anxiety on the acoustic blink reflex. Psychophysiology 28:588–595
Haggard P, Eimer M (1999) On the relation between brain potentials and the awareness of voluntary movements. Exp Brain Res 126:128–133
Ho KJ, Kileny P, Paccioretti D, McLean DR (1987) Neurologic, audiologic, and electrophysiologic sequelae of bitemporal lobe lesions. Arch Neurol 44:982–987
Hoffman HS, Fleshler M (1963) Startle reaction: modification by background acoustic stimulation. Science 141:928–930
Hoffman HS, Ison JR (1980) Reflex modification in the domain of startle:I. Some empirical findings and their implications for how the nervous system processes sensory input. Psychol Rev 87:175–189
Holand S, Girard A, Laude D, Meyer-Bisch C, Elghozi JL (1999) Effects of an auditory startle stimulus on blood pressure and heart rate in humans. J Hypertens 17:1893–1897
Hori A, Yasuhara A, Naito H, Yasuhara M (1986) Blink reflex elicited by auditory stimulation in the rabbit. J Neurol Sci 76:49–59
Inglis WL, Winn P (1995) The pedunculo-pontine tegmental nucleus: where the striatum meets the reticular formation. Prog Neurobiol 47:1–29
Ison JR, Hoffman HS (1983) Reflex modification in the domain of startle. II. The anomalous history of a robust and ubiquitous phenomenon. Psychol Bull 94:3–17
Ison JR, Sanes JN, Foss JA, Pinckney LA (1990) Facilitation and inhibition of the human startle blink reflexes by stimulus anticipation. Behav Neurosci 104:418–429
Jenny AB, Saper CB (1987) Organization of the facial nucleus and the corticofacial projection in the monkey: a reconsideration of the upper motor neuron facial palsy. Neurology 37:930–939
Koch M, Kungel M, Herbert H (1993) Cholinergic neurons in the pedunculopontine tegmental nucleus are involved in the mediation of prepulse inhibition of the acoustic startle response in the rat. Exp Brain Res 97:71–82
Koch M (1999) The neurobiology of startle. Progr Neurobiol 59:107–128
Kodsi MH, Swerdlow NR (1997) Regulation of prepulse inhibition by ventral pallidal projections. Brain Res Bull 43:219–228
Kofler M, Muller J, Reggiani L, Valls-Sole J (2001a) Influence of gender on auditory startle responses. Brain Res 921:206–210
Kofler M, Muller J, Reggiani L, Valls-Sole J (2001b) Influence of age on auditory startle responses in humans. Neurosci Lett 307:65–68
Kofler M, Müller J, Rinnerthaler-Weichbold M, Valls-Solé J (2008) Laterality of auditory startle responses in humans. Clin Neurophysiol 119:309–314
Kuhn AA, Sharott A, Trottenberg T, Kupsch A, Brown P (2004) Motor cortex inhibition induced by acoustic stimulation. Exp Brain Res 158:120–124
Kumru H, Urra X, Compta Y, Castellote JM, Turbau J, Valls-Sole J (2006) Excitability of subcortical motor circuits in Go/noGo and forced choice reaction time tasks. Neurosci Lett 406:66–70
Kumru H, Valls-Sole J (2006) Excitability of the pathways mediating the startle reaction before execution of a voluntary movement. Exp Brain Res 169:427–432
Landis C, Hunt WA (1939) The startle pattern. New York, Farrar, Strauss and Giroux
Lang PJ, Bradley MM, Cuthbert BN (1990) Emotion, attention and the startle reflex. Psychol Rev 97:377–395
Lang PJ, Davis M (2006) Emotion, motivation, and the brain:reflex foundations in animal and human research. Prog Brain Res 156:3–29
Lee Y, López DE, Meloni EJ, Davis M (1996) A primary acoustic startle pathway: obligatory role of cochlear root neurons and the nucleus reticularis pontis caudalis. J Neurosci 16:3775–3789
Libet B, Gleason CA, Wright EW, Pearl DK (1983) Time of conscious intention to act in relation to onset of cerebral activity (readiness-potential). Brain 106:623–642
Liegeois-Chauvel C, Morin C, Musolino A, Bancaud J, Chauvel P (1989) Evidence for contribution of the auditory cortex to audiospinal facilitation in man. Brain 112:375–391
Lingenhohl K, Friauf E (1994) Giant neurons in the rat reticular formation: a sensorimotor interface in the elementary acoustic startle circuit? J Neurosci 14:1176–1194
Lipp OV, Kaplan DM, Purkis HM (2006) Reaction time facilitation by acoustic task-irrelevant stimuli is not related to startle. Neurosci Lett 409:124–127
MacKinnon CD, Bissig D, Chiusano J, Miller E, Rudnick L, Jager C, Zhang Y, Mille ML, Rogers MW (2007) Preparation of anticipatory postural adjustments prior to stepping. J Neurophysiol 97:4368–4379
Matsumoto JY, Caviness JN, McEvoy KM (1994) The acoustic startle reflex in stiff-man syndrome. Neurology 44:1952–1955
McManis MH, Bradley MM, Berg WK, Cuthbert BN, Lang PJ (2001) Emotional reactions in children: verbal, physiological, and behavioral responses to affective pictures. Psychophysiology 8:222–231
Nickerson RS (1973) Intersensory facilitation of reaction time: energy summation or preparation enhancement? Psychol Rev 80:489–509
Nijhuis LB, Janssen L, Bloem BR, van Dijk JG, Gielen SC, Borm GF, Overeem S (2007) Choice reaction times for human head rotations are shortened by startling acoustic stimuli, irrespective of stimulus direction. J Physiol 584:97–109
Parent A, Hazrati LN (1995) Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain Res Brain Res Rev 20:128–154
Pascual-Leone A, Valls-Sole J, Wassermann EM, Brasil-Neto J, Cohen LG, Hallett M (1992) Effects of focal transcranial magnetic stimulation on simple reaction time to acoustic, visual and somatosensory stimuli. Brain 115:1045–1059
Paylor R, Crawley JN (1997) Inbred strain differences in prepulse inhibition of the mouse startle response. Psychopharmacology 132:169–180
Queralt A, Valls-Solé J, Castellote JM (2008) The effects of a startle on the sit-to-stand manoeuvre. Exp Brain Res 185:603–609
Reese NB, Garcia-Rill E, Skinner RD (1995) The pedunculopontine nucleus–auditory input, arousal and pathophysiology. Prog Neurobiol 47:105–133
Reynolds C, Ashby P (1999) Inhibition in the human motor cortex is reduced just before a voluntary contraction. Neurology 53:730–735
Reynolds RF, Day BL (2007) Fast visuomotor processing made faster by sound. J Physiol 583:1107–1115
Rossi A, Scarpini C (1992) Gating of trigemino-facial reflex from low-threshold trigeminal and extratrigeminal cutaneous fibres in humans. J Neurol Neurosurg Psychiatry 55:774–780
Sanegre MT, Castellote JM, Haggard P, Valls-Sole J (2004) The effects of a startle on awareness of action. Exp Brain Res 155:527–531
Schepens B, Drew T (2004) Independent and convergent signals from the pontomedullary reticular formation contribute to the control of posture and movement during reaching in the cat. J Neurophysiol 92:2217–2238
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
Starr A, Caramia M, Zarola F, Rossini PM (1988) Enhancement of motor cortical excitability in humans by non-invasive electrical stimulation appears prior to voluntary movement. Electroencephalogr Clin Neurophysiol 70:26–32
Swerdlow NR, Geyer MA (1993) Prepulse inhibition of acoustic startle in rats after lesions of the pedunculopontine tegmental nucleus. Behavioral Neuroscience 107:104–117
Swerdlow NR, Paulsen J, Braff DL, Butters N, Geyer MA, Swenson MR (1995) Impaired prepulse inhibition of acoustic and tactile startle response in patients with Huntington’s disease. J Neurol Neurosurg Psychiatry 58:192–200
Swerdlow NR, Braff DL, Geyer MA (2000) Animal models of deficient sensorimotor gating: what we know, what we think we know, and what we hope to know soon. Behav Pharmacol 11:185–204
Terao Y, Ugawa Y, Suzuki M, Sakai K, Hanajima R, Gemba-Shimizu K, Kanazawa I (1997) Shortening of simple reaction time by peripheral electrical and submotor-threshold magnetic cortical stimulation. Exp Brain Res 115:541–545
Timmann D, Musso C, Kolb FP, Rijntjes M, Jüptner M, Müller SP, Diener HC, Weiller C (1998) Involvement of the human cerebellum during habituation of the acoustic startle response: a PET study. J Neurol Neurosurg Psychiatry 65:771–773
Tresilian JR, Plooy AM (2006) Effects of acoustic startle stimuli on interceptive action. Neuroscience 142:579–594
Turpin G (1986) Effects of stimulus intensity on autonomic responding: The problem of differentiating orienting and defense reflexes. Psychophysiology 23:1–14
Valls-Solé J, Cammarota A, Alvarez R, Hallett M (1994) Orbicularis oculi responses to stimulation of nerve afferents from upper and lower limbs in normal humans. Brain Res 650:313–316
Valls-Solé J, Solé A, Valldeoriola F, Muñoz E, Gonzalez LE, Tolosa ES (1995) Reaction time and acoustic startle in normal human subjects. Neurosci Lett 195:97–100
Valls-Solé J, Valldeoriola F, Tolosa E, Nobbe F (1997) Habituation of the auditory startle reaction is reduced during preparation for execution of a motor task in normal human subjects. Brain Research 751:155–159
Valls-Solé J, Rothwell JC, Goulart F, Cossu G, Muñoz JE (1999a) Patterned ballistic movements triggered by a startle in healthy humans. J Physiol 516:931–938
Valls-Solé J, Valldeoriola F, Molinuevo JL, Cossu G, Nobbe F (1999b) Prepulse modulation of the startle reaction and the blink reflex in normal human subjects. Exp Brain Res 129:49–56
Valls-Solé J, Veciana M, León L, Valldeoriola F (2002) Effects of a startle on heart rate in patients with multiple system atrophy. Mov Disord 17:546–549
Valls-Sole J (2004) Contribution of subcortical motor pathways to the execution of ballistic movements. Suppl Clin Neurophysiol 57:554–562
Valls-Solé J, Kofler M, Kumru H, Castellote JM, Sanegre MT (2005) Startle-induced reaction time shortening is not modified by prepulse inhibition. Exp Brain Res 165:541–548
van Doornik J, Masakado Y, Sinkjaer T, Nielsen JB (2004) The suppression of the long-latency stretch reflex in the human tibialis anterior muscle by transcranial magnetic stimulation. Exp Brain Res 157:403–406
Walker DL, Davis M (1997) Anxiogenic effects of high illumination levels assessed with the acoustic startle response in rats. Biol Psychiatry 42:461–471
Wilkins DE, Hallett M, Wess MM (1986) Audiogenic startle reflex of man and its relationship to startle syndromes. Brain 109:561–573
Wu MF, Suzuki SS, Siegel JM (1988) Anatomical distribution and response patterns of reticular neurons active in relation to acoustic startle. Brain Res 457:399–406
Yeomans JS, Frankland PW (1996) The acoustic startle reflex: neurons and connections. Brain Res Rev 21:301–314
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Valls-Solé, J., Kumru, H. & Kofler, M. Interaction between startle and voluntary reactions in humans. Exp Brain Res 187, 497–507 (2008). https://doi.org/10.1007/s00221-008-1402-0
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DOI: https://doi.org/10.1007/s00221-008-1402-0