Tonic and phasic alertness training: a novel behavioral therapy to improve spatial and non-spatial attention in patients with hemispatial neglect

Joseph M Degutis, Thomas M Van Vleet, Joseph M Degutis, Thomas M Van Vleet

Abstract

Hemispatial neglect is a debilitating disorder marked by a constellation of spatial and non-spatial attention deficits. Patients' alertness deficits have shown to interact with lateralized attention processes and correspondingly, improving tonic/general alertness as well as phasic/moment-to-moment alertness has shown to ameliorate spatial bias. However, improvements are often short-lived and inconsistent across tasks and patients. In an attempt to more effectively activate alertness mechanisms by exercising both tonic and phasic alertness, we employed a novel version of a continuous performance task (tonic and phasic alertness training, TAPAT). Using a between-subjects longitudinal design and employing sensitive outcome measures of spatial and non-spatial attention, we compared the effects of 9 days of TAPAT (36 min/day) in a group of patients with chronic neglect (N = 12) with a control group of chronic neglect patients (N = 12) who simply waited during the same training period. Compared to the control group, the group trained on TAPAT significantly improved on both spatial and non-spatial measures of attention with many patients failing to exhibit a lateralized attention bias at the end of training. TAPAT was effective for patients with a range of behavioral profiles and lesions, suggesting that its effectiveness may rely on distributed or lower-level attention mechanisms that are largely intact in patients with neglect. In a follow-up experiment, to determine if TAPAT is more effective in improving spatial attention than an active treatment that directly trains spatial attention, we trained three chronic neglect patients on both TAPAT and search training. In all three patients, TAPAT training was more effective in improving spatial attention than search training suggesting that, in chronic neglect, training alertness is a more effective treatment approach than directly training spatial attention.

Keywords: attention; hemispatial neglect; neurological disorders; rehabilitation; visual.

Figures

Figure 1
Figure 1
MRI and CT scans of patients’ lesions in neurological convention (excluding patient JS).
Figure 2
Figure 2
TAPAT task. Each day, the training session began with the patients familiarizing themselves with a new target scene while reading the following instructions as the experimenter read them aloud: “You will see many scenes over the next 12 min. Your job is to hit the spacebar as fast as you can for each scene except when the scene is the target scene. When you see the target scene, do not hit the spacebar. The target scene for today is the following [Example Target Scene]. Please take a minute to memorize this scene.” Each 12-min round contained 360 trials: 36 target scenes (10%) and 324 non-target scenes (90%) randomly ordered. Each scene subtended a visual angle of 4° (vertical) × 6° (horizontal). On each trial, scenes were presented for 500 ms and between trials a blank screen with a fixation “+” at the center was shown for either 1000 ms (33.3% of trials), 1500 ms (33.3% of trials), or 2000 ms (33.3% of trials). After completion of a round of 360 trials, patients took a short break (approximately 2 min) before beginning the next 12-min round of 360 trials. Each day, patients performed three of these 12-min rounds for a total of 1080 trials.
Figure 3
Figure 3
Group (A) and individual (B) results of performance on the training task during the first and last day of training (error bars represent the standard error of the mean). There were no significant group changes with training (A), though individuals demonstrated significant improvements and decrements on different aspects of the training task (highlighted in gray and black). This was determined by performing Wilcoxon signed rank test on each component of training and assessing the calculated Z-score statistic at the p < 0.05 level.
Figure 4
Figure 4
Original conjunction search results for TAPAT group (A) and control group (B). The display time is the amount of time that the target (red square) had to be shown for patients to correctly identify it 75% of the time. This was calculated separately for right and left targets (error bars represent the standard error of the mean). (C) is an example of a left target present trial.
Figure 5
Figure 5
Alternative conjunction search results for TAPAT group. The display time is the amount of time that the target (blue triangle) had to be shown for patients to correctly identify it 75% of the time. This was calculated separately for right and left targets (error bars represent the standard error of the mean).
Figure 6
Figure 6
Group landmark results for TAPAT (A) and Control (B) groups. The pixel deviation from center measures patients’ subjective perception of the center of the black line compared to the actual center (left is negative, right is positive). Error bars represent the standard error of the mean. (C) is an example of a landmark display.
Figure 7
Figure 7
Group attentional blink results for TAPAT (A) and Control (B) groups. Correct Time 2 discrimination accuracy is the percentage of correct identifications of the second target (in the example, 7) when correctly identifying the first target (in the example, 3). This is calculated for when the second target lags the first target by two positions (see example) or six positions. Error bars represent the standard error of the mean. (C) is an example of a lag 2 attentional blink trial: 3 is the first target (T1) and 7 is the second target (T2).
Figure 8
Figure 8
Correlations between pre-training impairment and post-pre improvement scores for the original conjunction search (A), landmark task (B), and attentional blink task for lag 2 (C) and lag 6 (D).
Figure 9
Figure 9
Results of stepwise regressions predicting assessment improvement from training task improvement. (A) Shows the regression results predicting the post-pre improvement scores from improvements on components of the training task. ** indicates that the training component significantly predicted the particular assessment improvement (p<.05). (B–D) Show plots of the assessments with significant improvement-training component relationships.
Figure 10
Figure 10
Results of TAPAT training and search training in three chronic neglect patients for the conjunction search task and landmark task. Error bars represent the standard error of the mean. For the conjunction search, the display time is the amount of time that the target (red square) had to be shown for patients to correctly identify it 75% of the time. This was calculated separately for right and left targets. For the landmark task, pixel deviation was collapsed across right starting and left starting trials to give an average pixel deviation to the right (positive values) or left (negative values).

References

    1. Adair J. C., Barrett A. M. (2008). Spatial neglect: clinical and neuroscience review: a wealth of information on the poverty of spatial attention. Ann. N. Y. Acad. Sci. 1142, 21–4310.1196/annals.1444.008
    1. Aron A. R., Robbins T. W., Poldrack R. A. (2004). Inhibition and the right inferior frontal cortex. Trends Cogn. Sci. (Regul. Ed.) 8, 170–177
    1. Aston-Jones G., Cohen J. D. (2005). An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu. Rev. Neurosci. 28, 403–45010.1146/annurev.neuro.28.061604.135709
    1. Bartolomeo P. (2007). Visual neglect. Curr. Opin. Neurol. 20, 381–38610.1097/WCO.0b013e32816aa3a3
    1. Behrmann M., Ebert P., Black S. E. (2004). Hemispatial neglect and visual search: a large scale analysis. Cortex 40, 282–29010.1016/S0010-9452(08)70120-5
    1. Bellgrove M. A., Dockree P. M., Aimola L., Robertson I. H. (2004). Attenuation of spatial attentional asymmetries with poor sustained attention. Neuroreport 15, 1065–106910.1097/00001756-200404290-00027
    1. Beschin N., Robertson I. H. (1997). Personal versus extrapersonal neglect: a group study of their dissociation using a reliable clinical test. Cortex 33, 379–38410.1016/S0010-9452(08)70013-3
    1. Bisiach E., Perani D., Vallar G., Berti A. (1986). Unilateral neglect: personal and extra-personal. Neuropsychologia 24, 759–76710.1016/0028-3932(86)90075-8
    1. Boggio P. S., Nunes A., Rigonatti S. P., Nitsche M. A., Pascual-Leone A., Fregni F. (2007). Repeated sessions of noninvasive brain DC stimulation is associated with motor function improvement in stroke patients. Restor. Neurol. Neurosci. 25, 123–129
    1. Bouret S., Sara S. J. (2005). Network reset: a simplified overarching theory of locus coeruleus noradrenaline function. Trends Neurosci. 28, 574–58210.1016/j.tins.2005.09.002
    1. Brefczynski-Lewis J. A., Lutz A., Schaefer H. S., Levinson D. B., Davidson R. J. (2007). Neural correlates of attentional expertise in long-term meditation practitioners. Proc. Natl. Acad. Sci. U.S.A. 104, 11483.10.1073/pnas.0606552104
    1. Brighina F., Bisiach E., Oliveric M., Piazza A., La Bua V., Daniele O., Fierro B. (2003). 1 Hz repetitive transcranial magnetic stimulation of the unaffected hemisphere ameliorates contralesional visuospatial neglect in humans. Neurosci. Lett. 336, 131–13310.1016/S0304-3940(02)01283-1
    1. Buxbaum L. J., Ferraro M. K., Veramonti T., Farne A., Whyte J., Ladavas E., Frassinetti F., Coslett H. B. (2004). Hemispatial neglect: subtypes, neuroanatomy, and disability. Neurology 62, 749–756
    1. Corbetta M., Kincade M. J., Lewis C., Snyder A. Z., Sapir A. (2005). Neural basis and recovery of spatial attention deficits in spatial neglect. Nat. Neurosci. 8, 1603–161010.1038/nn1574
    1. Coull J. T., Nobre A. C., Frith C. D. (2001). The noradrenergic alpha2 agonist clonidine modulates behavioural and neuroanatomical correlates of human attentional orienting and alerting. Cereb Cortex. 11, 73–8410.1093/cercor/11.1.73
    1. Draganski B., May A. (2008). Training-induced structural changes in the adult human brain. Behav. Brain Res. 192, 137.10.1016/j.bbr.2008.02.015
    1. Fink G. R., Marshall J. C., Weiss P. H., Toni I., Zilles K. (2002). Task instructions influence the cognitive strategies involved in line bisection judgements: evidence from modulated neural mechanisms revealed by fMRI. Neuropsychologia 40, 119–13010.1016/S0028-3932(01)00087-2
    1. Halligan P. W., Marshall J. C. (1991). Left neglect for near but not far space in man. Nature 350, 498–50010.1038/350498a0
    1. Harvey M., Milner A. D., Roberts R. C. (1995). An investigation of hemispatial neglect using the Landmark Task. Brain Cogn. 27, 59–7810.1006/brcg.1995.1004
    1. Heilman K. M., Schwartz H. D., Watson R. T. (1978). Hypoarousal in patients with the neglect syndrome and emotional indifference. Neurology 28, 229–232
    1. Hjaltason H., Tegner R., Tham K., Levander M., Ericson K. (1996). Sustained attention and awareness of disability in chronic neglect. Neuropsychologia 34, 1229–123310.1016/0028-3932(96)00044-9
    1. Husain M., Rorden C. (2003). Non-spatially lateralized mechanisms in hemispatial neglect. Nat. Rev. Neurosci. 4, 26–3610.1038/nrn1005
    1. Husain M., Shapiro K., Martin J., Kennard C. (1997). Abnormal temporal dynamics of visual attention in spatial neglect patients. Nature 385, 154–15610.1038/385154a0
    1. Kaernbach C. (1990). A single-interval adjustment-matrix (SIAM) procedure for unbiased adaptive testing. J. Acoust. Soc. Am. 88, 2645–265510.1121/1.399985
    1. Katz N., Hartman-Maeir A., Ring H., Soroker N. (1999). Functional disability and rehabilitation outcome in right hemisphere damaged patients with and without unilateral spatial neglect. Arch. Phys. Med. Rehabil. 80, 379–38410.1016/S0003-9993(99)90273-3
    1. Kranczioch C., Debener S., Schwarzbach J., Goebel R., Engel A. K. (2005). Neural correlates of conscious perception in the attentional blink. Neuroimage 24, 704–71410.1016/j.neuroimage.2004.09.024
    1. Lazar R. M., Fitzsimmons B. F., Marshall R. S., Berman M. F., Bustillo M. A., Young W. L., Mohr J. P., Shah J., Robinson J. V. (2002). Reemergence of stroke deficits with midazolam challenge. Stroke 33, 283–28510.1161/hs0102.101222
    1. List A., Brooks J. L., Esterman M., Flevaris A. V., Landau A. N., Bowman G., Stanton V., Vanvleet T. M., Robertson L. C., Schendel K. (2008). Visual hemispatial neglect, re-assessed. J. Int. Neuropsychol. Soc. 14, 243–25610.1017/S1355617708080284
    1. Luaute J., Halligan P., Rode G., Rossetti Y., Boisson D. (2006). Visuo-spatial neglect: a systematic review of current interventions and their effectiveness. Neurosci. Biobehav. Rev. 30, 961–98210.1016/j.neubiorev.2006.03.001
    1. Malhotra P., Coulthard E. J., Husain M. (2009). Role of right posterior parietal cortex in maintaining attention to spatial locations over time. Brain 132, 645–66010.1093/brain/awn350
    1. Manly T., Dobler V. B., Dodds C. M., George M. A. (2005). Rightward shift in spatial awareness with declining alertness. Neuropsychologia 43, 1721–172810.1016/j.neuropsychologia.2005.02.009
    1. McGlinchey-Berroth R., Bullis D. P., Milberg W. P., Verfaellie M., Alexander M., D'Esposito M. (1996). Assessment of neglect reveals dissociable behavioral but not neuroanatomical subtypes. J. Int. Neuropsychol. Soc. 2, 441–45110.1017/S1355617700001521
    1. Naeser M. A., Martin P. I., Nicholas M., Baker E. H., Seekins H., Kobayashi M., Theoret H., Fregni F., Maria-Tormos J., Kurland J., Doron K. W., Pascual-Leone A. (2005). Improved picture naming in chronic aphasia after TMS to part of right Broca's area: an open-protocol study. Brain Lang. 93, 95–10510.1016/j.bandl.2004.08.004
    1. Nieuwenhuis S., Aston-Jones G., Cohen J. D. (2005). Decision making, the P3, and the locus coeruleus-norepinephrine system. Psychol. Bull. 131, 510–53210.1037/0033-2909.131.4.510
    1. Olk B., Wee J., Kingstone A. (2004). The effect of hemispatial neglect on the perception of centre. Brain Cogn. 55, 365–36710.1016/j.bandc.2004.02.048
    1. Ota H., Fijii T., Suzuki K., Fukatsu R., Yamadori A. (2001). Dissociation of body-centered and stimulus-centered representations in unilateral neglect. Neurology 57, 2064.
    1. Pizzamiglio L., Guariglia C., Antonucci G., Zoccolotti P. (2006). Development of a rehabilitative program for unilateral neglect. Restor. Neurol. Neurosci. 24, 337–345
    1. Posner M. I. (2008). Measuring Alertness. Ann. N. Y. Acad. Sci. 1129, 193–19910.1196/annals.1417.011
    1. Raymond J. E., Shapiro K. L., Arnell K. M. (1992). Temporary suppression of visual processing in an RSVP task: an attentional blink? J. Exp. Psychol. Hum. Percept. Perform. 18, 849–86010.1037/0096-1523.18.3.849
    1. Rensink R. A. (2002). Change detection. Annu. Rev. Psycholol. 53, 245–27710.1146/annurev.psych.53.100901.135125
    1. Robertson I. H. (2001). Do we need the “lateral” in unilateral neglect? Spatially nonselective attention deficits in unilateral neglect and their implications for rehabilitation. Neuroimage 14, S85–S9010.1006/nimg.2001.0838
    1. Robertson I. H., Manly T., Andrade J., Baddeley B. T., Yiend J. (1997a). ‘Oops!’: performance correlates of everyday attentional failures in traumatic brain injured and normal subjects. Neuropsychologia 35, 747–75810.1016/S0028-3932(97)00015-8
    1. Robertson I. H., Manly T., Beschin N., Daini R., Haeske-Dewick H., Hömberg V., Jehkonen M., Pizzamiglio G., Shiel A., Weber E. (1997b). Auditory sustained attention is a marker of unilateral spatial neglect. Neuropsychologia 35, 1527–153210.1016/S0028-3932(97)00084-5
    1. 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, 169–17210.1038/25993
    1. Robertson I. H., Tegner R., Tham K., Lo A., Nimmo-Smith I. (1995). Sustained attention training for unilateral neglect: theoretical and rehabilitation implications. J. Clin. Exp. Neuropsychol. 17, 416–43010.1080/01688639508405133
    1. Roth J. K., Serences J. T., Courtney S. M. (2006). Neural system for controlling the contents of object working memory in humans. Cereb. Cortex 16, 1595–160310.1093/cercor/bhj096
    1. Ryan M., Martin R., Denckla M. B., Mostofsky S. H., Mahone E. M. (2010). Interstimulus jitter facilitates response control in children with ADHD. J. Int. Neuropsychol. 16, 388–39310.1017/S1355617709991305
    1. Salthouse T. A. (2000). Aging and measures of processing speed. Biol. Psychol. 54, 35–5410.1016/S0301-0511(00)00052-1
    1. Schulz K. F., Grimes D. A. (2002). Generation of allocation sequences in randomised trials: chance, not choice. Lancet 359, 515–51910.1016/S0140-6736(02)07683-3
    1. Shapiro K. L., Raymond J. E., Arnell K. M. (1994). Attention to visual pattern information produces the attentional blink in rapid serial visual presentation. J. Exp. Psychol. Hum. Percept. Perform. 20, 357–37110.1037/0096-1523.20.2.357
    1. Smallwood J., Davies J. B., Heim D., Finnigan F., Sudberry M., O'Connor R., Obonsawin M. (2004). Subjective experience and the attentional lapse: task engagement and disengagement during sustained attention. Conscious. Cogn. 13, 657–69010.1016/j.concog.2004.06.003
    1. Sturm W., de Simone A., Krause B. J., Specht K., Hesselmann V., Radermacher I., Herzog H., Tellmann L., Müller-Gärtner H. W., Willmes K. (1999). Functional anatomy of intrinsic alertness: evidence for a fronto-parietal-thalamic-brainstem network in the right hemisphere. Neuropsychologia 37, 797–80510.1016/S0028-3932(98)00141-9
    1. Sturm W., Longoni F., Weis S., Specht K., Herzog H., Vohn R., Thimm M., Willmes K. (2004). Functional reorganisation in patients with right hemisphere stroke after training of alertness: a longitudinal PET and fMRI study in eight cases. Neuropsychologia 42, 434–45010.1016/j.neuropsychologia.2003.09.001
    1. Sturm W., Willmes K. (2001). On the functional neuroanatomy of intrinsic and phasic alertness. Neuroimage 14(Pt 2), S76–S8410.1006/nimg.2001.0839
    1. Tang Y. Y., Posner M. I. (2009). Attention training and attention state training. Trends Cogn. Sci. (Regul. Ed.) 13, 222–227
    1. Thiel C. M., Zilles K., Fink G. R. (2004). Cerebral correlates of alerting, orienting and reorienting of visuospatial attention: an event-related fMRI study. Neuroimage 21, 318–32810.1016/j.neuroimage.2003.08.044
    1. 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, 1230–124610.1016/j.neuropsychologia.2005.09.008
    1. Toraldo A., McIntosh R. D., Dijkerman H. C., Milner A. D. (2004). A revised method for analysing neglect using the landmark task. Cortex 40, 415–43110.1016/S0010-9452(08)70136-9
    1. Van Vleet T. M., Robertson L. C. (2006). Cross-modal interactions in time and space: auditory influence on visual attention in hemispatial neglect. J. Cogn. Neurosci. 18, 1368–137910.1162/jocn.2006.18.8.1368
    1. Wilcoxon F. (1945). Individual comparisons by ranking methods. Biometrics 1, 80–8310.2307/3001968
    1. Young A. W., Hellawell D. J., Welch J. (1992). Neglect and visual recognition. Brain 115(Pt 1), 51–7110.1093/brain/115.1.51

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