Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-05T07:58:35.135Z Has data issue: false hasContentIssue false

Differential Effects of Lowered Arousal on Covert and Overt Shifts of Attention

Published online by Cambridge University Press:  15 June 2015

Bruno Fimm*
Affiliation:
RWTH Aachen University, Department of Neurology, Section Neuropsychology, Aachen
Klaus Willmes
Affiliation:
RWTH Aachen University, Department of Neurology, Section Neuropsychology, Aachen
Will Spijkers
Affiliation:
RWTH Aachen University, Institute of Psychology, Aachen
*
Correspondence and reprint requests to: Bruno Fimm, RWTH Aachen University, Department of Neurology, Section Neuropsychology, Pauwelsstraße 30, D-52074 Aachen. E-mail: [email protected]

Abstract

Based on previous studies demonstrating detrimental effects of reduced alertness on attentional orienting our study seeks to examine covert and overt attentional orienting in different arousal states. We hypothesized an attentional asymmetry with increasing reaction times to stimuli presented to the left visual field in a state of maximally reduced arousal. Eleven healthy participants underwent sleep deprivation and were examined repeatedly every 4 hr over 28 hr in total with two tasks measuring covert and overt orienting of attention. Contrary to our hypothesis, a reduction of arousal did not induce any asymmetry of overt orienting. Even in participants with profound and significant attentional asymmetries in covert orienting no substantial reaction time differences between left- and right-sided targets in the overt orienting task could be observed. This result is not in agreement with assumptions of a tight coupling of covert and overt attentional processes. In conclusion, we found differential effects of lowered arousal induced by sleep deprivation on covert and overt orienting of attention. This pattern of results points to a neuronal non-overlap of brain structures subserving these functions and a differential influence of the norepinephrine system on these modes of spatial attention. (JINS, 2015, 21, 545–557)

Type
Research Articles
Copyright
Copyright © The International Neuropsychological Society 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Asanowicz, D., Marzecová, A., Jaśkowski, P., & Wolski, P. (2012). Hemispheric asymmetry in the efficiency of attentional networks. Brain and Cognition, 79(2), 117128. doi:10.1016/j.bandc.2012.02.014 Google Scholar
Aston-Jones, G., & Cohen, J.D. (2005). An integrative theory of locus coeruleus-norepinephrine function: Adaptive gain and optimal performance. Annual Review of Neuroscience, 28, 403450. doi:10.1146/annurev.neuro.28.061604.135709 Google Scholar
Bareham, C.A., Manly, T., Pustovaya, O.V., Scott, S.K., & Bekinschtein, T.A. (2014). Losing the left side of the world: Rightward shift in human spatial attention with sleep onset. Scientific Reports, 4, doi:10.1038/srep05092 Google Scholar
Bartolomeo, P., & Chokron, S. (2002). Orienting of attention in left unilateral neglect. Neuroscience and Biobehavioral Reviews, 26(2), 217234.Google Scholar
Beauchamp, M.S., Petit, L., Ellmore, T.M., Ingeholm, J., & Haxby, J.V. (2001). A parametric fmri study of overt and covert shifts of visuospatial attention. Neuroimage, 14(2), 310321. doi:10.1006/nimg.2001.0788 CrossRefGoogle ScholarPubMed
Benwell, C.S., Harvey, M., Gardner, S., & Thut, G. (2013). Stimulus- and state-dependence of systematic bias in spatial attention: Additive effects of stimulus-size and time-on-task. Cortex, 49(3), 827836. doi:10.1016/j.cortex.2011.12.007 Google Scholar
Bundesen, C. (1998). A computational theory of visual attention. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 353(1373), 12711281. doi:10.1098/rstb.1998.0282 Google Scholar
Chica, A.B., Thiebaut de Schotten, M., Toba, M., Malhotra, P., Lupiáñez, J., & Bartolomeo, P. (2012). Attention networks and their interactions after right-hemisphere damage. Cortex, 48(6), 654663. doi:10.1016/j.cortex.2011.01.009 Google Scholar
Corbetta, M., & Shulman, G.L. (1998). Human cortical mechanisms of visual attention during orienting and search. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 353(1373), 13531362. doi:10.1098/rstb.1998.0289 Google Scholar
Corbetta, M., & Shulman, G.L. (2011). Spatial neglect and attention networks. Annual Review of Neuroscience, 34, 569599. doi:10.1146/annurev-neuro-061010-113731 Google Scholar
Coull, J.T. (1998). Neural correlates of attention and arousal: Insights from electrophysiology, functional neuroimaging and psychopharmacology. Progress in Neurobiology, 55(4), 343361.Google Scholar
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. Clinical Neurophysiology, 111(10), 17711778.Google Scholar
de Haan, B., Morgan, P.S., & Rorden, C. (2008). Covert orienting of attention and overt eye movements activate identical brain regions. Brain Research, 1204, 102111. doi:10.1016/j.brainres.2008.01.105 CrossRefGoogle ScholarPubMed
Dobler, V.B., Manly, T., Verity, C., Woolrych, J., & Robertson, I.H. (2003). Modulation of spatial attention in a child with developmental unilateral neglect. Developmental Medicine & Child Neurology, 45(4), 282288.Google Scholar
Dodds, C.M., van Belle, J., Peers, P.V., Dove, A., Cusack, R., Duncan, J., & Manly, T. (2008). The effects of time-on-task and concurrent cognitive load on normal visuospatial bias. Neuropsychology, 22(4), 545552. doi:10.1037/0894-4105.22.4.545 Google Scholar
Dodds, C., Müller, U., & Manly, T. (2009). Effects of psychostimulants on alertness and spatial bias in healthy participants. Journal of Cognitive Neuroscience, 21(3), 529537. doi:10.1162/jocn.2009.21046 Google Scholar
Doricchi, F., Thiebaut de Schotten, M., Tomaiuolo, F., & Bartolomeo, P. (2008). White matter (dis)connections and gray matter (dys)functions in visual neglect: Gaining insights into the brain networks of spatial awareness. Cortex, 44(8), 983995. doi:10.1016/j.cortex.2008.03.006 CrossRefGoogle ScholarPubMed
Dufour, A., Touzalin, P., & Candas, V. (2007). Time-on-task effect in pseudoneglect. Experimental Brain Research, 176(3), 532537. doi:10.1007/s00221-006-0810-2 Google Scholar
Edgington, E.S., & Onghena, P. (2007). Randomization tests (4th ed.). Boca Raton: Chapman & Hall/CRC.Google Scholar
Fellrath, J., Blanche-Durbec, V., Schnider, A., Jacquemoud, A.-S., & Ptak, R. (2012). Visual search in spatial neglect studied with a preview paradigm. Frontiers in Human Neuroscience, 6, 93. doi:10.3389/fnhum.2012.00093 Google Scholar
Fimm, B., Willmes, K., & Spijkers, W. (2006). The effect of low arousal on visuo-spatial attention. Neuropsychologia, 44(8), 12611268. doi:10.1016/j.neuropsychologia.2006.01.027 Google Scholar
Fink, G.R., Marshall, J.C., Weiss, P.H., & Zilles, K. (2001). The neural basis of vertical and horizontal line bisection judgments: An fMRI study of normal volunteers. Neuroimage, 14(1 Pt 2), S59S67. doi:10.1006/nimg.2001.0819 Google Scholar
Finke, K., Matthias, E., Keller, I., Müller, H.J., Schneider, W.X., & Bublak, P. (2012). How does phasic alerting improve performance in patients with unilateral neglect? A systematic analysis of attentional processing capacity and spatial weighting mechanisms. Neuropsychologia, 50, 11781189. doi:10.1016/j.neuropsychologia.2012.02.008 CrossRefGoogle ScholarPubMed
Fransson, P.A., 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. Journal of Vestibular Research: Equilibrium & Orientation, 18(4), 209222.Google Scholar
Harvey, M., Olk, B., Muir, K., & Gilchrist, I.D. (2002). Manual responses and saccades in chronic and recovered hemispatial neglect: A study using visual search. Neuropsychologia, 40(7), 705717.Google Scholar
Hildebrandt, H., Giesselmann, H., & Sachsenheimer, W. (1999). Visual search and visual target detection in patients with infarctions of the left or right posterior or the right middle brain artery. Journal of Clinical and Experimental Neuropsychology, 21(1), 94107.Google Scholar
Hopfinger, J.B., Camblin, C.C., & Parks, E.L. (2010). Isolating the internal in endogenous attention. Psychophysiology, 47(4), 739747. doi:10.1111/j.1469-8986.2010.00981.x Google Scholar
Jewell, G., & McCourt, M.E. (2000). Pseudoneglect: A review and meta-analysis of performance factors in line bisection tasks . Neuropsychologia, 38, 93110.Google Scholar
Kirk, R.E. (2012). Experimental design: Procedures of the behavioral sciences (4th ed.). Thousand Oaks: Sage Publications.Google Scholar
Klein, R.M., & Lawrence, M.A. (2012). On the modes and domains of attention. In M.I. Posner (Ed.), Cognitive neuroscience of attention (2nd ed., pp. 1128). New York, NY: Guilford Press.Google Scholar
Manly, T., Cornish, K., Grant, C., Dobler, V., & Hollis, C. (2005a). Examining the relationship between rightward visuo-spatial bias and poor attention within the normal child population using a brief screening task. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 46(12), 13371344. doi:10.1111/j.1469-7610.2005.01432.x Google Scholar
Manly, T., Dobler, V.B., Dodds, C.M., & George, M.A. (2005b). Rightward shift in spatial awareness with declining alertness. Neuropsychologia, 43(12), 17211728. doi:10.1016/j.neuropsychologia.2005.02.009 Google Scholar
Matthias, E., Bublak, P., Costa, A., Müller, H.J., Schneider, W.X., & Finke, K. (2009). Attentional and sensory effects of lowered levels of intrinsic alertness. Neuropsychologia, 47(14), 32553264. doi:10.1016/j.neuropsychologia.2009.08.004 Google Scholar
Mesulam, M.M. (1999). Spatial attention and neglect: Parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. Philosophical Transactions of the Royal Society B: Biological Sciences, 354(1387), 13251346. doi:10.1098/rstb.1999.0482 Google Scholar
Natale, E., Marzi, C.A., Bricolo, E., Johannsen, L., & Karnath, H.-O. (2007). Abnormally speeded saccades to ipsilesional targets in patients with spatial neglect. Neuropsychologia, 45(2), 263272. doi:10.1016/j.neuropsychologia.2006.07.008 Google Scholar
Newman, D.P., O’Connell, R.G., & Bellgrove, M.A. (2003). Linking time-on-task, spatial bias and hemispheric activation asymmetry: A neural correlate of rightward attention drift. Neuropsychologia, 51(7), 12151223.Google Scholar
Nobre, A.C., Gitelman, D.R., Dias, E.C., & Mesulam, M.M. (2000). Covert visual spatial orienting and saccades: Overlapping neural systems. Neuroimage, 11(3), 210216. doi:10.1006/nimg.2000.0539 Google Scholar
Olk, B., Harvey, M., & Gilchrist, I.D. (2002). First saccades reveal biases in recovered neglect. Neurocase, 8(4), 306313. doi:10.1076/neur.8.3.306.16191 Google Scholar
Petersen, S.E., & Posner, M.I. (2012). The attention system of the human brain: 20 years after. Annual Review of Neuroscience, 35, 7389. doi:10.1146/annurev-neuro-062111-150525 Google Scholar
Posner, M.I. (1980). Orienting of attention. The Quarterly Journal of Experimental Psychology, 32(1), 325. doi:10.1080/00335558008248231 Google Scholar
Posner, M.I. (2008). Measuring alertness. Annals of the New York Academy of Sciences, 1129, 193199. doi:10.1196/annals.1417.011 Google Scholar
Pouget, P., Stepniewska, I., Crowder, E.A., Leslie, M.W., Emeric, E.E., Nelson, M.J., & Schall, J.D. (2009). Visual and motor connectivity and the distribution of calcium-binding proteins in macaque frontal eye field: Implications for saccade target selection. Frontiers in Neuroanatomy, 3, 2. doi:10.3389/neuro.05.002.2009 Google Scholar
Rizzolatti, G., Riggio, L., Dascola, I., & Umiltà, C. (1987). Reorienting attention across the horizontal and vertical meridians: Evidence in favor of a premotor theory of attention. Neuropsychologia, 25(1A), 3140.CrossRefGoogle ScholarPubMed
Robertson, I.H., Mattingley, J.B., Rorden, C., & Driver, J. (1998). Phasic alerting of neglect patients overcomes their spatial deficit in visual awareness. Nature, 395(6698), 169172. doi:10.1038/25993 Google Scholar
Robertson, I., Hogg, K., & McMillan, T. (1998). Rehabilitation of unilateral neglect: Improving function by contralesional limb activation. Neuropsychological Rehabilitation, 8, 1930.Google Scholar
Robertson, I., Tegner, R., Tham, K., Lo, A., & Nimmo-Smith, I. (1995). Sustained attention training for unilateral neglect - theoretical and rehabilitation implications. Journal of Clinical and Experimental Neuropsychology, 17(3), 416430.Google Scholar
Robinson, R.G. (1985). Lateralized behavior and neurochemical consequences of unilateral brain injury in rats. In S.D. Glick (Ed.), Cerebral lateralization in nonhuman species (pp 135156). New York: Academic Press.Google Scholar
Russo, M., Thomas, M., Thorne, D., Sing, H., Redmond, D., Rowland, L., & Balkin, T. (2003). Oculomotor impairment during chronic partial sleep deprivation. Clinical Neurophysiology, 114(4), 723736.Google Scholar
Samuels, E.R., & Szabadi, E. (2008). Functional neuroanatomy of the noradrenergic locus coeruleus: Its roles in the regulation of arousal and autonomic function part II: Physiological and pharmacological manipulations and pathological alterations of locus coeruleus activity in humans. Current Neuropharmacology, 6(3), 254285. doi:10.2174/157015908785777193 Google Scholar
Schall, J.D., & Thompson, K.G. (2012). Neural mechanisms of saccade target selection. In M.I. Posner (Ed.), Cognitive neuroscience of attention (2nd ed., pp. 242256). New York, NY: Guilford Press.Google Scholar
Schmidt, C., Collette, F., Cajochen, C., & Peigneux, P. (2007). A time to think: Circadian rhythms in human cognition. Cognitive Neuropsychology, 24(7), 755789. doi:10.1080/02643290701754158 Google Scholar
Schmitz, R., Deliens, G., Mary, A., Urbain, C., & Peigneux, P. (2011). Selective modulations of attentional asymmetries after sleep deprivation. Neuropsychologia, 49(12), 33513360. doi:10.1016/j.neuropsychologia.2011.08.009 Google Scholar
Shulman, G.L., & Corbetta, M. (2012). Two attentional networks. Identification and function within a larger cognitive architecture. In M.I. Posner (Ed.), Cognitive neuroscience of attention. (2nd ed. pp. 113128). New York: The Guilford Press.Google Scholar
Shulman, G.L., Pope, D.L.W., Astafiev, S.V., McAvoy, M.P., Snyder, A.Z., & Corbetta, M. (2010). Right hemisphere dominance during spatial selective attention and target detection occurs outside the dorsal frontoparietal network. The Journal of Neuroscience, 30(10), 36403651. doi:10.1523/JNEUROSCI.4085-09.2010 Google Scholar
Sommer, M.A., & Wurtz, R.H. (2000). Composition and topographic organization of signals sent from the frontal eye field to the superior colliculus. Journal of Neurophysiology, 83(4), 19792001.Google Scholar
Sturm, W., & Willmes, K. (2001). On the functional neuroanatomy of intrinsic and phasic alertness. Neuroimage, 14(1 Pt 2), S76S84. doi:10.1006/nimg.2001.0839 Google Scholar
Thimm, M., Fink, G.R., Küst, J., Karbe, H., & Sturm, W. (2006). Impact of alertness training on spatial neglect: A behavioural and fMRI study. Neuropsychologia, 44(7), 12301246. doi:10.1016/j.neuropsychologia.2005.09.008 Google Scholar
Thimm, M., Fink, G.R., Küst, J., Karbe, H., Willmes, K., & Sturm, W. (2009). Recovery from hemineglect: Differential neurobiological effects of optokinetic stimulation and alertness training. Cortex, 45(7), 850862. doi:10.1016/j.cortex.2008.10.007 Google Scholar
Vallar, G. (2001). Extrapersonal visual unilateral spatial neglect and its neuroanatomy. Neuroimage, 14(1 Pt 2), S52S58. doi:10.1006/nimg.2001.0822 Google Scholar
Vossel, S., Weidner, R., Driver, J., Friston, K.J., & Fink, G.R. (2012). Deconstructing the architecture of dorsal and ventral attention systems with dynamic causal modeling. The Journal of Neuroscience, 32(31), 1063710648. doi:10.1523/JNEUROSCI.0414-12.2012 Google Scholar
Zils, E., Sprenger, A., Heide, W., Born, J., & Gais, S. (2005). Differential effects of sleep deprivation on saccadic eye movements. Sleep, 28(9), 11091115.Google Scholar