Abstract
Attention plays a critical role in action selection. However, the role of attention in eye movements is complicated as these movements can be either voluntary or involuntary, with, in some circumstances (antisaccades), these two actions competing with each other for execution. But attending to the location of an impending eye movement is only one facet of attention that may play a role in eye movement selection. In two experiments, we investigated the effect of arousal on voluntary eye movements (antisaccades) and involuntary eye movements (prosaccadic errors) in an antisaccade task. Arousal, as caused by brief loud sounds and indexed by changes in pupil diameter, had a facilitation effect on involuntary eye movements. Involuntary eye movements were both significantly more likely to be executed and significantly faster under arousal conditions (Experiments 1 and 2), and the influence of arousal had a specific time course (Experiment 2). Arousal, one form of attention, can produce significant costs for human movement selection as potent but unplanned actions are benefited more than planned ones.
Similar content being viewed by others
Notes
After completion of this experiment, participants also completed an additional experiment of 96 trials of the same task without warning signals and were asked to rate if they made an error and how confident they were in that judgment. This data was obtained for a different purpose from the present paper.
References
Bernstein IH, Rose R, Ashe V (1970) Preparatory state effects in intersensory facilitation. Psychon Sci 19:113–114
Blaukopf CL, DiGirolamo GJ (2005) The automatic extraction and use of information from cues and go signals in an antisaccade task. Exp Brain Res 167:654–659
Blaukopf CL, DiGirolamo GJ (2006) Differential effects of reward and punishment on conscious and unconscious eye movements. Exp Brain Res 174:786–792
Blaukopf CL, DiGirolamo GJ (2007) Reward, context & human behaviour. Sci World J 7:626–640
Bohlin G, Graham FK (1977) Cardiac deceleration and reflex blink facilitation. Psychophysiology 14:423–431
Bowditch HP, Warren JW (1890) The knee-jerk reaction and its modifications. J Physiol 11:25–64
Bradley MM, Miccoli L, Escrig MA, Lang PJ (2008) The pupil as a measure of emotional arousal and autonomic activation. Psychophysiology 45:602–607
Calvo MG, Lang PJ (2005) Parafoveal semantic processing of emotional visual scenes. J Exp Psychol Hum Percept and Perform 31:502–519
Chen B, May PJ (2000) The feedback circuit connecting the superior colliculus and the central mesencephalic reticular formation: a direct morphological demonstration. Exp Brain Res 131:10–21
Chen XY, Wolpaw JR (1995) Operant conditioning of the H-reflex in freely moving rats. J Neurophysiol 73:411–415
Corbetta M, Akbudak E, Conturo TE et al (1998) A common network of functional areas for attention and eye movements. Neuron 21:761–773
Deuter CE, Schilling TM, Kuehl LK, Blumenthal TD, Schachniger H (2013) Startle effects on saccadic responses to emotional stimuli. Psychophysiology 50:1056–1063
DiGirolamo GJ, Smelson D, Guevremont N (2015) Cue-Induced craving in patients with cocaine use disorder predicts cognitive control deficits toward cocaine cues. Addict Behav 47:86–90
DiGirolamo GJ, Sophis EJ, Daffron JL, Gonzalez G, Romero-Gonzalez M, Gillespie SA (2016) Breakdowns of eye movement control toward smoking cues in young adult light smokers. Addict Behav 52:98–102
Duncan J (2006) Brain mechanisms of attention. Q J Exp Psychol 59:2–27
Evdokimidis I, Smyrnis N, Constantinidis TS et al (2002) The antisaccade task in a sample of 2,006 young men. I. Normal population characteristics. Exp Brain Res 147:45–52
Fischer B, Weber H (1996) Effects of procues on error rate and reaction time of antisaccades in human subjects. Exp Brain Res 109:507–512
Fischer B, Gezeck S, Mokler A (1999) Erroneous prosaccades in a gap-antisaccade-task. In: Becker W, Deubel H, Mergner T (eds) Current oculomotor research: physiological and psychological aspects. Plenum Publishers, New York, pp 53–63
Foltz EL, Schmidt RP (1956) The role of the reticular formation in the coma of head injury. J Neurosurg 13:145–154
Hackley S (2009) The speeding of voluntary reaction by a warning signal. Psychophysiology 46:225–233
Hackley SA, Valle-Inclan F (1999) Accessory stimulus effects on response selection: does arousal speed decision making? J Cogn Neurosci 11:321–329
Hallett PE (1978) Primary and secondary saccades to goals defined by instructions. Vis Res 18:1279–1296
Kirchner H, Colonius H (2005) Cognitive control can modulate intersensory facilitation: speeding up visual antisaccades with an auditory distracter. Exp Brain Res 166:440–444
Kissler J, Keil A (2008) Look–don’t look! How emotional pictures affect pro-and anti-saccades. Exp Brain Res 188:215–222
Klein RM (1980) Does oculormotor readiness mediate cognitive control of visual attention? In: Nickerson R (ed) Attention and Performance. Lawrence Erlbaum Associates, Hillsdale, pp 259–276
Klein TA, Endrass T, Kathmann K, Neumann J, von Cramon DY, Ullsperger M (2007) Neural correlates of awareness. Neuroimage 34:1774–1781
Kristjánsson Á, Chen Y, Nakayama K (2001) Less attention is more in the preparation of antisaccades, but not prosaccades. Nat Neurosci 4:1037–1042
Kristjánsson A, Vandenbroucke MWG, Driver J (2004) When pros become cons for anti- versus prosaccades: factors with opposite or common effects on different saccade types. Exp Brain Res 155:231–244
LaBar KS, Mesulam M, Gitelman DR, Weintraub S (2000) Emotional curiosity: modulation of visuospatial attention by arousal is preserved in aging and early-stage Alzheimer’s disease. Neuropsychologia 38:1734–1740
Lang PJ, Bradley MM, Cuthbert BN (2008) International affective picture system (IAPS): affective ratings of pictures and instruction manual. Technical Report A-8. University of Florida, Gainesville, FL
Low KA, Larson SL, Burke J, Hackley SA (1996) Alerting effects on choice reaction time and the photic eyeblink reflex. Electroencephalogr Clin Neurophysiol 98:385–393
Massen C (2004) Parallel programming of exogenous and endogenous components in the antisaccade task. Q J Exp Psychol Sect A 57:475–498
Milstein DM, Dorris MC (2007) The influence of expected value on saccadic preparation. J Neurosci 27:4810–4818
Mort DJ, Perry RJ, Mannan SK et al (2003) Differential cortical activation during voluntary and reflexive saccades in man. Neuroimage 18:231–246
Munk MHJ, Roelfsema PR, König P, Engel AK, Singer W (1996) Role of reticular activation in the modulation of intracortical synchronization. Science 272:271–274
Munoz DP, Everling S (2004) Look away: the anti-saccade task and the voluntary control of eye movement. Nat Rev Neurosci 5:218–228
Posner MI (1978) Chronometric explorations of mind. Erlbaum, Hillsdale
Posner MI, Boies SJ (1971) Components of attention. Psychol Rev 78:391–408
Posner MI, DiGirolamo GJ (1998) Executive attention: conflict, target detection and cognitive control. In: Parasuraman R (ed) The attentive brain. MIT Press, Cambridge, pp 401–423
Posner MI, DiGirolamo GJ (1999) Attention in cognitive neuroscience. In: Gazzaniga M (ed) The cognitive neurosciences, 2nd edn. MIT Press, Cambridge, pp 623–631
Rizzolatti G, Riggio L, Dascola I, Umilta C (1987) Reorienting attention across the horizontal and vertical meridians: evidence in favor of a premotor theory of attention. Neuropsychologia 25:31–40
Robbins TW, Everitt BJ (1995) Arousal systems and attention. In: Gazzaniga M (ed) The cognitive neurosciences. MIT Press, Cambridge, pp 703–720
Stahl J, Rammsayer TH (2005) Accessory stimulation in the time course of visuomotor information processing: stimulus intensity effects on reaction time and response force. Acta Psychol 120:1–18
van Steenbergen H et al (2011) Threat but not arousal narrows attention: evidence from pupil dilation and saccade control. Front Psychol 2:281. doi:10.3389/fpsyg.2011.00281
Wenban-Smith MG, Findlay JM (1991) Express saccades: is there a separate population in humans? Exp Brain Res 87:218–222
Yerkes RM, Dodson JD (1908) The relation of strength of stimulus to rapidity of habit-formation. J Comp Neurol Psychol 18:459–482
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
DiGirolamo, G.J., Patel, N. & Blaukopf, C.L. Arousal facilitates involuntary eye movements. Exp Brain Res 234, 1967–1976 (2016). https://doi.org/10.1007/s00221-016-4599-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-016-4599-3