The effects of enhanced attention and working memory on smooth pursuit eye movement

Abstract

It has long been suggested that increasing attentional demands can alter smooth pursuit eye movements, but the precise nature of the changes generated is not clear. Our goal was to examine smooth pursuit with a task that enhanced attention to the target and that increased demands on working memory, without distracting from the target. 15 subjects tracked a target moving around a predictable circular trajectory at a constant tangential velocity. An n-back task with two levels of additional working memory load was integrated into the pursuit target to increase cognitive demands. In the single-task conditions, subjects either performed pursuit alone or the n-back task with a stationary target. In the dual-task conditions, pursuit and the n-back task were performed together. Performance of the n-back tasks was not impaired by simultaneous smooth pursuit. The n-back tasks had negligible effects on horizontal or vertical pursuit gain, but generated increased phase lag and reduced the variability of position error during pursuit. Increasing the difficulty of the n-back task further reduced the variability of position errors. We conclude that enhanced attention does not alter the velocity gain of smooth pursuit but rather improves its consistency. As long as attention remains focused on the target, increased attentional demands further reduce pursuit variability. Increases in phase lag may serve to improve attentional processing of the target.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Acker W, Toone B (1978) Attention, eye tracking and schizophrenia. Br J Soc Clin Psychol 17:173–181

    CAS  Article  PubMed  Google Scholar 

  2. Baird B, Smallwood J, Lutz A, Schooler JW (2014) The decoupled mind: mind-wandering disrupts cortical phase-locking to perceptual events. J Cogn Neurosci 26:2596–2607. https://doi.org/10.1162/jocn_a_00656

    Article  PubMed  Google Scholar 

  3. Barnes G (2008) Cognitive processes involved in smooth pursuit eye movements. Brain Cogn 68:309–326. https://doi.org/10.1016/j.bandc.2008.08.020

    CAS  Article  PubMed  Google Scholar 

  4. Bartolomeo P, Sieroff E, Chokron S, Decaix C (2001) Variability of response times as a marker of diverted attention. Neuropsychologia 39:358–363

    CAS  Article  PubMed  Google Scholar 

  5. Brezinova V, Kendell RE (1977) Smooth pursuit eye movements of schizophrenics and normal people under stress. Br J Psychiatry 130:59–63

    CAS  Article  PubMed  Google Scholar 

  6. Castellanos FX, Sonuga-Barke EJ, Milham MP, Tannock R (2006) Characterizing cognition in ADHD: beyond executive dysfunction. Trends Cogn Sci 10:117–123. https://doi.org/10.1016/j.tics.2006.01.011

    Article  PubMed  Google Scholar 

  7. Cegalis JA, Hafez H, Wong PS (1983) What is deviant about deviant smooth pursuit eye movements in schizophrenia? Psychiatry Res 10:47–58

    CAS  Article  PubMed  Google Scholar 

  8. Chen J, Valsecchi M, Gegenfurtner K (2017) Attention is allocated closely ahead of the target during smooth pursuit eye movements: evidence from EEG frequency tagging. Neuropsychologia 102:206–216. https://doi.org/10.1016/j.neuropsychologia.2017.06.024

    Article  PubMed  Google Scholar 

  9. Clementz BA, Sweeney JA, Hirt M, Haas G (1990) Pursuit gain and saccadic intrusions in first-degree relatives of probands with schizophrenia. J Abnorm Psychol 99:327–335

    CAS  Article  PubMed  Google Scholar 

  10. Contreras R, Ghajar J, Bahar S, Suh M (2011) Effect of cognitive load on eye-target synchronization during smooth pursuit eye movement. Brain Res 1398:55–63. https://doi.org/10.1016/j.brainres.2011.05.004

    CAS  Article  PubMed  Google Scholar 

  11. Hutton S, Tegally D (2005) The effects of dividing attention on smooth pursuit eye tracking. Exp Brain Res 163:306–313. https://doi.org/10.1007/s00221-004-2171-z

    CAS  Article  PubMed  Google Scholar 

  12. Iacono WG, Tuason VB, Johnson RA (1981) Dissociation of smooth-pursuit and saccadic eye tracking in remitted schizophrenics. An ocular reaction time task that schizophrenic perform well. Arch Gen Psychiatry 38:991–996

    CAS  Article  PubMed  Google Scholar 

  13. Iacono WG, Peloquin LJ, Lumry AE, Valentine RH, Tuason VB (1982) Eye tracking in patients with unipolar and bipolar affective disorders in remission. J Abnorm Psychol 91:35–44

    CAS  Article  PubMed  Google Scholar 

  14. Jaeggi S, Buschkuehl M, Perrig W, Meier B (2010) The concurrent validity of the N-back task as a working memory measure. Memory 18:394–412. https://doi.org/10.1080/09658211003702171

    Article  PubMed  Google Scholar 

  15. Kathmann N, Hochrein A, Uwer R (1999) Effects of dual task demands on the accuracy of smooth pursuit eye movements. Psychophysiology 36:158–163. https://doi.org/10.1017/S0048577299981167

    CAS  Article  PubMed  Google Scholar 

  16. Kaufman SR, Abel LA (1986) The effects of distraction on smooth pursuit in normal subjects. Acta Otolaryngol 102:57–64

    CAS  Article  PubMed  Google Scholar 

  17. Kerzel D, Ziegler N (2005) Visual short-term memory during smooth pursuit eye movements. J Exp Psychol Hum Percept Perform 31:354–372. https://doi.org/10.1037/0096-1523.31.2.354

    Article  PubMed  Google Scholar 

  18. Kerzel D, Born S, Souto D (2009) Smooth pursuit eye movements and perception share target selection, but only some central resources. Behav Brain Res 201:66–73. https://doi.org/10.1016/j.bbr.2009.01.032

    Article  PubMed  Google Scholar 

  19. Khan A, Lefèvre P, Heinen S, Blohm G (2010) The default allocation of attention is broadly ahead of smooth pursuit. J Vis 10:7. https://doi.org/10.1167/10.13.7

    Article  PubMed  Google Scholar 

  20. Kowler E (2011) Eye movements: the past 25 years. Vis Res 51:1457–1483. https://doi.org/10.1016/j.visres.2010.12.014

    Article  PubMed  PubMed Central  Google Scholar 

  21. Krauzlis RJ, Miles FA (1996) Initiation of saccades during fixation or pursuit: evidence in humans for a single mechanism. J Neurophysiol 76:4175–4179

    CAS  Article  PubMed  Google Scholar 

  22. Lipton RB, Frost LA, Holzman PS (1980) Smooth pursuit eye movements, schizophrenia, and distraction. Percept Mot Skills 50:159–167. https://doi.org/10.2466/pms.1980.50.1.159

    CAS  Article  PubMed  Google Scholar 

  23. Lisberger SG, Morris EJ, Tychsen L (1987) Visual motion processing and sensory-motor integration for smooth pursuit eye movements. Annu Rev Neurosci 10:97–129. https://doi.org/10.1146/annurev.ne.10.030187.000525

    CAS  Article  PubMed  Google Scholar 

  24. Lovejoy LP, Fowler GA, Krauzlis RJ (2009) Spatial allocation of attention during smooth pursuit eye movements. Vis Res 49:1275–1285. https://doi.org/10.1016/j.visres.2009.01.011

    Article  PubMed  PubMed Central  Google Scholar 

  25. Lutz A, Slagter HA, Rawlings NB, Francis AD, Greischar LL, Davidson RJ (2009) Mental training enhances attentional stability: neural and behavioral evidence. J Neurosci 29:13418–13427. https://doi.org/10.1523/JNEUROSCI.1614-09.2009

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  26. Maruta J, Suh M, Niogi SN, Mukherjee P, Ghajar J (2010) Visual tracking synchronization as a metric for concussion screening. J Head Trauma Rehabilit 25:293–305. https://doi.org/10.1097/HTR.0b013e3181e67936

    Article  Google Scholar 

  27. Maruta J, Heaton K, Kryskow E, Maule A, Ghajar J (2013) Dynamic visuomotor synchronization: quantification of predictive timing. Behav Res Methods 45:289–300. https://doi.org/10.3758/s13428-012-0248-3

    Article  PubMed  Google Scholar 

  28. Pavel M (1990) Predictive control of eye movement. In: Kowler E (ed) Eye movements and their role in visual and cognitive processes. Elsevier, Amsterdam, pp 71–114

    Google Scholar 

  29. Rubia K, Taylor A, Taylor E, Sergeant JA (1999) Synchronization, anticipation, and consistency in motor timing of children with dimensionally defined attention deficit hyperactivity behaviour. Percept Mot Skills 89:1237–1258. https://doi.org/10.2466/pms.1999.89.3f.1237

    CAS  Article  PubMed  Google Scholar 

  30. Schuirmann DJ (1987) A comparison of the two one-sided tests procedure and the power approach for assessing the equivalence of average bioavailability. J Pharmacokinet Biopharm 15:657–680

    CAS  Article  PubMed  Google Scholar 

  31. Shagass C, Richard R, Amadeo M (1976) Eye-tracking performance and engagement of attention. Arch Gen Psychiatry 33:121–125

    CAS  Article  PubMed  Google Scholar 

  32. Sharpe JA, Sylvester TO (1978) Effect of aging on horizontal smooth pursuit. Invest Ophthalmol Vis Sci 17:465–468

    CAS  PubMed  Google Scholar 

  33. Spohn HE, Coyne L, Spray J (1988) The effect of neuroleptics and tardive dyskinesia on smooth-pursuit eye movement in chronic schizophrenics. Arch Gen Psychiatry 45:833–840

    CAS  Article  PubMed  Google Scholar 

  34. Spooner J, Sakala S, Baloh R (1980) Effect of aging on eye tracking. Arch Neurol 37:575–576

    CAS  Article  PubMed  Google Scholar 

  35. Stuss DT, Stethem LL, Hugenholtz H, Picton T, Pivik J, Richard MT (1989) Reaction time after head injury: fatigue, divided and focused attention, and consistency of performance. J Neurol Neurosurg Psychiatry 52:742–748

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. Stuss DT, Murphy KJ, Binns MA, Alexander MP (2003) Staying on the job: the frontal lobes control individual performance variability. Brain 126:2363–2380. https://doi.org/10.1093/brain/awg237

    Article  PubMed  Google Scholar 

  37. Sweeney JA, Clementz BA, Haas GL, Escobar MD, Drake K, Frances AJ (1994) Eye tracking dysfunction in schizophrenia: characterization of component eye movement abnormalities, diagnostic specificity, and the role of attention. J Abnorm Psychol 103:222–230

    CAS  Article  PubMed  Google Scholar 

  38. Tanaka M, Yoshida T, Fukushima K (1998) Latency of saccades during smooth-pursuit eye movement in man. Directional asymmetries. Exp Brain Res 121:92–98

    CAS  Article  PubMed  Google Scholar 

  39. van Donkelaar P (1999) Spatiotemporal modulation of attention during smooth pursuit eye movements. Neuroreport 10:2523–2526

    Article  PubMed  Google Scholar 

  40. Van Gelder P, Anderson S, Herman E, Lebedev S, Tsui WH (1990) Saccades in pursuit eye tracking reflect motor attention processes. Compr Psychiatry 31:253–260

    Article  PubMed  Google Scholar 

  41. Van Gelder P, Lebedev S, Liu P, Tsui W (1995) Anticipatory saccades in smooth pursuit: task effects and pursuit vector after saccades. Vis Res 35:667–678

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Miriam Spering for helpful discussions. JJSB was supported by a Canada Research Chair (950-228984) and the Marianne Koerner Chair in Brain Diseases. SLC was supported by the National Eye Institute of the National Institutes of Health under award number F32 EY023479. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Author information

Affiliations

Authors

Contributions

JLS, SLC, WJP, and JJSB conceptualized the experiment and BK assisted with computer programming. JLS conducted the testing of participants, pursuit analysis, and wrote the initial draft. JJSB performed the statistical analysis. All authors contributed to the interpretation of results, writing and approval of the final draft.

Corresponding author

Correspondence to Jacob L. Stubbs.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Stubbs, J.L., Corrow, S.L., Kiang, B. et al. The effects of enhanced attention and working memory on smooth pursuit eye movement. Exp Brain Res 236, 485–495 (2018). https://doi.org/10.1007/s00221-017-5146-6

Download citation

Keywords

  • Ocular motor
  • Velocity gain
  • Phase
  • Consistency
  • Variability
  • n-Back