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Published in: Experimental Brain Research 1/2014

01-01-2014 | Research Article

Adaptation of visual tracking synchronization after one night of sleep deprivation

Authors: Jianliang Tong, Jun Maruta, Kristin J. Heaton, Alexis L. Maule, Jamshid Ghajar

Published in: Experimental Brain Research | Issue 1/2014

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Abstract

The temporal delay between sensory input and motor execution is a fundamental constraint in interactions with the environment. Predicting the temporal course of a stimulus and dynamically synchronizing the required action with the stimulus are critical for offsetting this constraint, and this prediction–synchronization capacity can be tested using visual tracking of a target with predictable motion. Although the role of temporal prediction in visual tracking is assumed, little is known of how internal predictions interact with the behavioral outcome or how changes in the cognitive state influence such interaction. We quantified and compared the predictive visual tracking performance of military volunteers before and after one night of sleep deprivation. The moment-to-moment synchronization of visual tracking during sleep deprivation deteriorated with sensitivity changes greater than 40 %. However, increased anticipatory saccades maintained the overall temporal accuracy with near zero phase error. Results suggest that acute sleep deprivation induces instability in visuomotor prediction, but there is compensatory visuomotor adaptation. Detection of these visual tracking features may aid in the identification of insufficient sleep.
Literature
go back to reference Asmussen G, Gaunitz U (1981) Mechanical properties of the isolated inferior oblique muscle of the rabbit. Pflugers Arch 392:183–190PubMedCrossRef Asmussen G, Gaunitz U (1981) Mechanical properties of the isolated inferior oblique muscle of the rabbit. Pflugers Arch 392:183–190PubMedCrossRef
go back to reference Barmack NH, Bell CC, Rence BG (1971) Tension and rate of tension development during isometric responses of extraocular muscle. J Neurophysiol 34:1072–1079PubMed Barmack NH, Bell CC, Rence BG (1971) Tension and rate of tension development during isometric responses of extraocular muscle. J Neurophysiol 34:1072–1079PubMed
go back to reference Barnes GR (2008) Cognitive processes involved in smooth pursuit eye movements. Brain Cogn 68:309–326PubMedCrossRef Barnes GR (2008) Cognitive processes involved in smooth pursuit eye movements. Brain Cogn 68:309–326PubMedCrossRef
go back to reference Behrens F, Mackeben M, Schröder-Preikschat W (2010) An improved algorithm for automatic detection of saccades in eye movement data and for calculating saccade parameters. Behav Res Methods 42:701–708PubMedCrossRef Behrens F, Mackeben M, Schröder-Preikschat W (2010) An improved algorithm for automatic detection of saccades in eye movement data and for calculating saccade parameters. Behav Res Methods 42:701–708PubMedCrossRef
go back to reference Bocca ML, Denise P (2006) Total sleep deprivation effect on disengagement of spatial attention as assessed by saccadic eye movements. Clin Neurophysiol 117:894–899PubMedCrossRef Bocca ML, Denise P (2006) Total sleep deprivation effect on disengagement of spatial attention as assessed by saccadic eye movements. Clin Neurophysiol 117:894–899PubMedCrossRef
go back to reference Chee MW, Goh CS, Namburi P, Parimal S, Seidl KN, Kastner S (2011) Effects of sleep deprivation on cortical activation during directed attention in the absence and presence of visual stimuli. Neuroimage 58:595–604PubMedCentralPubMedCrossRef Chee MW, Goh CS, Namburi P, Parimal S, Seidl KN, Kastner S (2011) Effects of sleep deprivation on cortical activation during directed attention in the absence and presence of visual stimuli. Neuroimage 58:595–604PubMedCentralPubMedCrossRef
go back to reference Chen Y, Holzman PS, Nakayama K (2002) Visual and cognitive control of attention in smooth pursuit. Prog Brain Res 140:255–265PubMedCrossRef Chen Y, Holzman PS, Nakayama K (2002) Visual and cognitive control of attention in smooth pursuit. Prog Brain Res 140:255–265PubMedCrossRef
go back to reference Collewijn H, Tamminga EP (1984) Human smooth and saccadic eye movements during voluntary pursuit of different target motions on different backgrounds. J Physiol 24:1789–1898 Collewijn H, Tamminga EP (1984) Human smooth and saccadic eye movements during voluntary pursuit of different target motions on different backgrounds. J Physiol 24:1789–1898
go back to reference Coppe S, Orban de Xivry JJ, Yüksel D, Ivanoiu A, Lefèvre P (2012) Dramatic impairment due to frontal lobe degeneration. J Neurophysiol 25:293–305 Coppe S, Orban de Xivry JJ, Yüksel D, Ivanoiu A, Lefèvre P (2012) Dramatic impairment due to frontal lobe degeneration. J Neurophysiol 25:293–305
go back to reference Corbetta M, Akbudak E, Conturo TE, Snyder AZ et al (1998) A common network of functional areas for attention and eye movements. Neuron 21:761–773PubMedCrossRef Corbetta M, Akbudak E, Conturo TE, Snyder AZ et al (1998) A common network of functional areas for attention and eye movements. Neuron 21:761–773PubMedCrossRef
go back to reference De Gennaro L, Ferrara M, Urbani L, Bertini M (2000) Oculomotor impairment after 1 night of total sleep deprivation: a dissociation between measures of speed and accuracy. Clin Neurophysiol 111:1771–1778PubMedCrossRef De Gennaro L, Ferrara M, Urbani L, Bertini M (2000) Oculomotor impairment after 1 night of total sleep deprivation: a dissociation between measures of speed and accuracy. Clin Neurophysiol 111:1771–1778PubMedCrossRef
go back to reference de Hann B, Morgan PS, Rorden C (2008) Covert orienting of attention and overt eye movements activate identical brain regions. Brain Res 1204:102–111CrossRef de Hann B, Morgan PS, Rorden C (2008) Covert orienting of attention and overt eye movements activate identical brain regions. Brain Res 1204:102–111CrossRef
go back to reference Forest G, Godbout R (2000) Effects of sleep deprivation on performance and EEG spectral analysis in young adults. Brain Cogn 43:195–200PubMed Forest G, Godbout R (2000) Effects of sleep deprivation on performance and EEG spectral analysis in young adults. Brain Cogn 43:195–200PubMed
go back to reference Fransson PA, Patel M, Magnusson M, Berg S, Almbladh P, Gomez S (2008) Effects of 24-hour and 36-hour sleep deprivation on smooth pursuit and saccadic eye movements. J Vestib Res 18:209–222PubMed Fransson PA, Patel M, Magnusson M, Berg S, Almbladh P, Gomez S (2008) Effects of 24-hour and 36-hour sleep deprivation on smooth pursuit and saccadic eye movements. J Vestib Res 18:209–222PubMed
go back to reference Friedman L, Jesberger JA, Meltzer HY (1991) A model of smooth pursuit performance illustrates the relationship between gain, catch-up saccade rate, and catch-up saccade amplitude in normal controls and patients with schizophrenia. Biol Psychiatry 30:537–556PubMedCrossRef Friedman L, Jesberger JA, Meltzer HY (1991) A model of smooth pursuit performance illustrates the relationship between gain, catch-up saccade rate, and catch-up saccade amplitude in normal controls and patients with schizophrenia. Biol Psychiatry 30:537–556PubMedCrossRef
go back to reference Gazes Y, Bakitin BC, Steffener J, Habeck C et al (2012) Dual-tasking alleviated sleep deprivation disruption in visuomotor tracking: an fMRI study. Brain Cogn 78:248–256PubMedCentralPubMedCrossRef Gazes Y, Bakitin BC, Steffener J, Habeck C et al (2012) Dual-tasking alleviated sleep deprivation disruption in visuomotor tracking: an fMRI study. Brain Cogn 78:248–256PubMedCentralPubMedCrossRef
go back to reference Ghajar J, Ivry RB (2009) The predictive brain state: asynchrony in disorders of attention? Neuroscientist 15:232–242PubMedCrossRef Ghajar J, Ivry RB (2009) The predictive brain state: asynchrony in disorders of attention? Neuroscientist 15:232–242PubMedCrossRef
go back to reference Goldich Y, Barkana Y, Pras E, Zadok D et al (2010) The effects of sleep deprivation on oculomotor responses. Curr Eye Res 35:1135–1141PubMedCrossRef Goldich Y, Barkana Y, Pras E, Zadok D et al (2010) The effects of sleep deprivation on oculomotor responses. Curr Eye Res 35:1135–1141PubMedCrossRef
go back to reference Grace PM, Stanford T, Gentgall M, Rolan PE (2010) Utility of saccadic eye movement analysis as an objective biomarker to detect the sedative interaction between opioids and sleep deprivation in opioid-naïve and opioid-tolerant populations. J Psychopharmacol 24:1631–1640PubMedCrossRef Grace PM, Stanford T, Gentgall M, Rolan PE (2010) Utility of saccadic eye movement analysis as an objective biomarker to detect the sedative interaction between opioids and sleep deprivation in opioid-naïve and opioid-tolerant populations. J Psychopharmacol 24:1631–1640PubMedCrossRef
go back to reference Khan AZ, Lefèvre P, Heinen SJ, Blohm G (2010) The default allocation of attention is broadly ahead of smooth pursuit. J Vis 10:7PubMedCrossRef Khan AZ, Lefèvre P, Heinen SJ, Blohm G (2010) The default allocation of attention is broadly ahead of smooth pursuit. J Vis 10:7PubMedCrossRef
go back to reference Konen CS, Kastner S (2008) Representation of eye movements and stimulus motion in topographically organized areas of human posterior parietal cortex. J Neurosci 28:8361–8375PubMedCentralPubMedCrossRef Konen CS, Kastner S (2008) Representation of eye movements and stimulus motion in topographically organized areas of human posterior parietal cortex. J Neurosci 28:8361–8375PubMedCentralPubMedCrossRef
go back to reference Lencer R, Trillenberg P (2008) Neurophysiology and neuroanatomy of smooth pursuit in humans. Brain Cogn 68:219–228PubMedCrossRef Lencer R, Trillenberg P (2008) Neurophysiology and neuroanatomy of smooth pursuit in humans. Brain Cogn 68:219–228PubMedCrossRef
go back to reference Maruta J, Suh M, Niogi SN, Mukherjee P, Ghajar J (2010) Visual tracking synchronization as a metric for concussion screening. J Head Trauma Rehabil 25:293–305PubMedCrossRef Maruta J, Suh M, Niogi SN, Mukherjee P, Ghajar J (2010) Visual tracking synchronization as a metric for concussion screening. J Head Trauma Rehabil 25:293–305PubMedCrossRef
go back to reference Maruta J, Heaton KJ, Kryskow EM, Maule AL, Ghajar J (2013) Dynamic visuomotor synchronization: quantification of predictive timing. Behav Res Methods 45:289–300PubMedCentralPubMedCrossRef Maruta J, Heaton KJ, Kryskow EM, Maule AL, Ghajar J (2013) Dynamic visuomotor synchronization: quantification of predictive timing. Behav Res Methods 45:289–300PubMedCentralPubMedCrossRef
go back to reference Miyata S, Noda A, Ozaki N, Hara Y et al (2010) Insufficient sleep impairs driving performance and cognitive function. Neurosci Lett 469:229–233PubMedCrossRef Miyata S, Noda A, Ozaki N, Hara Y et al (2010) Insufficient sleep impairs driving performance and cognitive function. Neurosci Lett 469:229–233PubMedCrossRef
go back to reference Mustari MJ, Ono S, Das VE (2009) Signal processing and distribution in cortical-brainstem pathways for smooth pursuit eye movements. Ann N Y Acad Sci 1164:147–154PubMedCentralPubMedCrossRef Mustari MJ, Ono S, Das VE (2009) Signal processing and distribution in cortical-brainstem pathways for smooth pursuit eye movements. Ann N Y Acad Sci 1164:147–154PubMedCentralPubMedCrossRef
go back to reference Nyström M, Holmqvist K (2010) An adaptive algorithm for fixation, saccade, and glissade detection in eyetracking data. Behav Res Methods 42:188–204PubMedCrossRef Nyström M, Holmqvist K (2010) An adaptive algorithm for fixation, saccade, and glissade detection in eyetracking data. Behav Res Methods 42:188–204PubMedCrossRef
go back to reference Orban de Xivry J–J, Lefevre P (2009) Interactions between saccades and pursuit. In: Squire LR (ed) Encyclopedia of neuroscience. Academic Press, Oxford Orban de Xivry J–J, Lefevre P (2009) Interactions between saccades and pursuit. In: Squire LR (ed) Encyclopedia of neuroscience. Academic Press, Oxford
go back to reference Osborne LC, Lisberger SG, Bialek W (2005) A sensory source for motor variation. Nature 437:412–416PubMedCrossRef Osborne LC, Lisberger SG, Bialek W (2005) A sensory source for motor variation. Nature 437:412–416PubMedCrossRef
go back to reference Porcu S, Ferrara M, Urbani L, Bellatreccia A, Casagrande M (1998) Smooth pursuit and saccadic eye movements as possible indicators of nighttime sleepiness. Physiol Behav 65:437–443PubMedCrossRef Porcu S, Ferrara M, Urbani L, Bellatreccia A, Casagrande M (1998) Smooth pursuit and saccadic eye movements as possible indicators of nighttime sleepiness. Physiol Behav 65:437–443PubMedCrossRef
go back to reference Poudel GR, Jones RD, Innes CR, Watts R (2009) fMRI correlates of behavioural microsleeps during a continuous visuomotor task. Conf Proc IEEE Eng Med Biol Soc 2009:2919–2922PubMed Poudel GR, Jones RD, Innes CR, Watts R (2009) fMRI correlates of behavioural microsleeps during a continuous visuomotor task. Conf Proc IEEE Eng Med Biol Soc 2009:2919–2922PubMed
go back to reference Rashbass C (1961) The relationship between saccadic and smooth tracking eye movements. J Physiol 159:326–338PubMed Rashbass C (1961) The relationship between saccadic and smooth tracking eye movements. J Physiol 159:326–338PubMed
go back to reference Rothenberg S, Schottenfeld S, Selkoe D, Gross K (1980) Specific oculomotor deficit after acute methadone. II. Smooth pursuit eye movements. Psychopharmacology 67:229–234PubMedCrossRef Rothenberg S, Schottenfeld S, Selkoe D, Gross K (1980) Specific oculomotor deficit after acute methadone. II. Smooth pursuit eye movements. Psychopharmacology 67:229–234PubMedCrossRef
go back to reference Rowland LM, Thomas ML, Thorne DR, Sing HC et al (2005) Oculomotor responses during partial and total sleep deprivation. Aviat Space Environ Med 76:C104–C113PubMed Rowland LM, Thomas ML, Thorne DR, Sing HC et al (2005) Oculomotor responses during partial and total sleep deprivation. Aviat Space Environ Med 76:C104–C113PubMed
go back to reference Russo M, Thomas M, Thorne D, Sing H et al (2003) Oculomotor impairment during chronic partial sleep deprivation. Clin Neurophysiol 114:723–736PubMedCrossRef Russo M, Thomas M, Thorne D, Sing H et al (2003) Oculomotor impairment during chronic partial sleep deprivation. Clin Neurophysiol 114:723–736PubMedCrossRef
go back to reference Schluppeck D, Glimcher P, Heeger DJ (2005) Topographic organization for delayed saccades in human posterior parietal cortex. J Neurophysiol 94:1372–1384PubMedCentralPubMedCrossRef Schluppeck D, Glimcher P, Heeger DJ (2005) Topographic organization for delayed saccades in human posterior parietal cortex. J Neurophysiol 94:1372–1384PubMedCentralPubMedCrossRef
go back to reference Spering M, Carrasco M (2012) Similar effects of feature-based attention on motion perception and pursuit eye movements at different levels of awareness. J Neurosci 32:7594–7601PubMedCentralPubMedCrossRef Spering M, Carrasco M (2012) Similar effects of feature-based attention on motion perception and pursuit eye movements at different levels of awareness. J Neurosci 32:7594–7601PubMedCentralPubMedCrossRef
go back to reference Stark L, Vossius G, Young LR (1962) Predictive control of eye tracking movements. IRE Trans Hum Factors Electron 2:52–57CrossRef Stark L, Vossius G, Young LR (1962) Predictive control of eye tracking movements. IRE Trans Hum Factors Electron 2:52–57CrossRef
go back to reference Tanaka M (2005) Involvement of the central thalamus in the control of smooth pursuit eye movements. J Neurosci 25:5866–5876PubMedCrossRef Tanaka M (2005) Involvement of the central thalamus in the control of smooth pursuit eye movements. J Neurosci 25:5866–5876PubMedCrossRef
go back to reference Tavassoli A, Ringach DL (2009) Dynamics of smooth pursuit maintenance. J Neurophysiol 102:110–118PubMedCrossRef Tavassoli A, Ringach DL (2009) Dynamics of smooth pursuit maintenance. J Neurophysiol 102:110–118PubMedCrossRef
go back to reference Thomas M, Sing H, Belenky G, Holcomb H et al (2000) Neural basis of alertness and cognitive performance impairments during sleepiness. I. Effects of 24 hours of sleep deprivation on waking human regional brain activity. J Sleep Res 9:335–352PubMedCrossRef Thomas M, Sing H, Belenky G, Holcomb H et al (2000) Neural basis of alertness and cognitive performance impairments during sleepiness. I. Effects of 24 hours of sleep deprivation on waking human regional brain activity. J Sleep Res 9:335–352PubMedCrossRef
go back to reference Tomasi D, Wang RL, Telang F, Boronikolas V et al (2009) Impairment of attentional networks after 1 night of sleep deprivation. Cereb Cortex 19:233–240PubMedCrossRef Tomasi D, Wang RL, Telang F, Boronikolas V et al (2009) Impairment of attentional networks after 1 night of sleep deprivation. Cereb Cortex 19:233–240PubMedCrossRef
go back to reference Van Gelder P, Lebedev S, Liu PM, Tsui WH (1995) Anticipatory saccades in smooth pursuit: task effects and pursuit vector after saccades. Vision Res 35:667–678PubMedCrossRef Van Gelder P, Lebedev S, Liu PM, Tsui WH (1995) Anticipatory saccades in smooth pursuit: task effects and pursuit vector after saccades. Vision Res 35:667–678PubMedCrossRef
go back to reference Wang P, Nikolić D (2011) An LCD monitor with sufficiently precise timing for research in vision. Front Hum Neurosci 5:85PubMedCentralPubMed Wang P, Nikolić D (2011) An LCD monitor with sufficiently precise timing for research in vision. Front Hum Neurosci 5:85PubMedCentralPubMed
go back to reference Westheimer G (1954) Eye movement responses to a horizontally moving visual stimulus. AMA Arch Ophthalmol 52:932–941PubMedCrossRef Westheimer G (1954) Eye movement responses to a horizontally moving visual stimulus. AMA Arch Ophthalmol 52:932–941PubMedCrossRef
go back to reference Wu JC, Gillin JC, Buchsbaum MS, Chen P et al (2006) Frontal lobe metabolic decreases with sleep deprivation not totally reversed by recovery sleep. Neuropsychopharmacology 31:2783–2792PubMedCrossRef Wu JC, Gillin JC, Buchsbaum MS, Chen P et al (2006) Frontal lobe metabolic decreases with sleep deprivation not totally reversed by recovery sleep. Neuropsychopharmacology 31:2783–2792PubMedCrossRef
go back to reference Yoshida A, Tanaka M (2009) Neuronal activity in the primate globus pallidus during smooth pursuit eye movements. NeuroReport 20:121–125PubMedCrossRef Yoshida A, Tanaka M (2009) Neuronal activity in the primate globus pallidus during smooth pursuit eye movements. NeuroReport 20:121–125PubMedCrossRef
go back to reference Zils E, Sprenger A, Heide W, Born J, Gais S (2005) Differential effects of sleep deprivation on saccadic eye movements. Sleep 28:1109–1115PubMed Zils E, Sprenger A, Heide W, Born J, Gais S (2005) Differential effects of sleep deprivation on saccadic eye movements. Sleep 28:1109–1115PubMed
Metadata
Title
Adaptation of visual tracking synchronization after one night of sleep deprivation
Authors
Jianliang Tong
Jun Maruta
Kristin J. Heaton
Alexis L. Maule
Jamshid Ghajar
Publication date
01-01-2014
Publisher
Springer Berlin Heidelberg
Published in
Experimental Brain Research / Issue 1/2014
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-013-3725-8

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