Korean Journal of Biological Psychiatry (생물정신의학)

The Korean Society of Biological Psychiatry (대한생물정신의학회)
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Potential Significance of Eyeblinks as a Behavior Marker of Neuropsychiatric Disorders

눈깜박임의 정신질환 행동지표로서의 가능성에 대한 고찰

  • Received : 2011.10.04
  • Accepted : 2011.11.07
  • Published : 2012.02.29
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Abstract

The primary purpose of this review is to present an overview of relationship between human spontaneous eyeblinking and internal cognitive processes. The second purpose is to address the neural substrates of human eyeblinking based on recent studies focusing on the central dopaminergic system and to explore the significance of spontaneous eyeblinks in neuropsychiatric disorders. We reviewed recent and previous studies on eyeblink patterns under various cognitive tasks. We also reviewed neural substrates of eyeblinking, particularly based on the central dopaminergic system. This paper suggests that spontaneous eyeblinks are highly correlated with various cognitive processes and the activity of central dopaminergic system. Various neuropsychiatric disorders are related to the alteration of the occurrence of eyeblinking. Spontaneous eyeblinking is the unique human behavior that occurs regularly without conscious effort. It is known that the rate of eyeblinking is modulated by internal cognitive processes and dopamine-related neuropsychiatric disorders. Further research is required to how the temporal dynamics of spontaneous eyeblinking is correlated with the disease activity and progression.

Keywords

References

  1. Zametkin AJ, Stevens JR, Pittman R. Ontogeny of spontaneous blinking and of habituation of the blink reflex. Ann Neurol 1979;5:453-457. https://doi.org/10.1002/ana.410050509
  2. Lawrenson JG, Birhah R, Murphy PJ. Tear-film lipid layer morphology and corneal sensation in the development of blinking in neonates and infants. J Anat 2005;206:265-270. https://doi.org/10.1111/j.1469-7580.2005.00386.x
  3. Lozato PA, Pisella PJ, Baudouin C. [The lipid layer of the lacrimal tear film: physiology and pathology]. J Fr Ophtalmol 2001;24:643-658.
  4. Lemp MA, Hamill JR Jr. Factors affecting tear film breakup in normal eyes. Arch Ophthalmol 1973;89:103-105. https://doi.org/10.1001/archopht.1973.01000040105007
  5. Vanley GT, Leopold IH, Gregg TH. Interpretation of tear film breakup. Arch Ophthalmol 1977;95:445-448. https://doi.org/10.1001/archopht.1977.04450030087010
  6. Doane MG. Interactions of eyelids and tears in corneal wetting and the dynamics of the normal human eyeblink. Am J Ophthalmol 1980;89:507-516. https://doi.org/10.1016/0002-9394(80)90058-6
  7. Ponder E. Kennedy W. On the act of blinking. Quarterly Journal of Physiology 1928;18:11.
  8. Isenberg SJ, Del Signore M, Chen A, Wei J, Guillon JP. The lipid layer and stability of the preocular tear film in newborns and infants. Ophthalmology 2003;110:1408-1411. https://doi.org/10.1016/S0161-6420(03)00451-2
  9. Bacher LF, Smotherman WP. Spontaneous eye blinking in human infants: a review. Dev Psychobiol 2004;44:95-102. https://doi.org/10.1002/dev.10162
  10. Stern JA, Walrath LC, Goldstein R. The endogenous eyeblink. Psychophysiology 1984;21:22-33. https://doi.org/10.1111/j.1469-8986.1984.tb02312.x
  11. Doughty MJ. Consideration of three types of spontaneous eyeblink activity in normal humans: during reading and video display terminal use, in primary gaze, and while in conversation. Optom Vis Sci 2001;78:712-725. https://doi.org/10.1097/00006324-200110000-00011
  12. De Jong PJ, Merckelbach H. Eyeblink frequency, rehearsal activity, and sympathetic arousal. Int J Neurosci 1990;51:89-94. https://doi.org/10.3109/00207459009000513
  13. von Cramon D, Schuri U. Blink frequency and speed motor activity. Neuropsychologia 1980;18:603-606. https://doi.org/10.1016/0028-3932(80)90164-5
  14. Karson CN. Spontaneous eye-blink rates and dopaminergic systems. Brain 1983;106:643-653. https://doi.org/10.1093/brain/106.3.643
  15. Karson CN, Berman KF, Donnelly EF, Mendelson WB, Kleinman JE, Wyatt RJ. Speaking, thinking, and blinking. Psychiatry Res 1981;5:243-246. https://doi.org/10.1016/0165-1781(81)90070-6
  16. Freed WJ, Kleinman JE, Karson CN, Potkin SG, Murphy DL, Wyatt RJ. Eye-blink rates and platelet monoamine oxidase activity in chronic schizophrenic patients. Biol Psychiatry 1980;15:329-332.
  17. Deuschl G, Goddemeier C. Spontaneous and reflex activity of facial muscles in dystonia, Parkinson's disease, and in normal subjects. J Neurol Neurosurg Psychiatry 1998;64:320-324. https://doi.org/10.1136/jnnp.64.3.320
  18. Aqur AMR, Dalley AF. Grant's Atlas of Anatomy. 12th Edition. Philadelphia: Lippincott Williams & Wilkins;2008.
  19. Dimitrova A, Weber J, Maschke M, Elles HG, Kolb FP, Forsting M, et al. Eyeblink-related areas in human cerebellum as shown by fMRI. Hum Brain Mapp 2002;17:100-115. https://doi.org/10.1002/hbm.10056
  20. Tsubota K, Kwong KK, Lee TY, Nakamura J, Cheng HM. Functional MRI of brain activation by eye blinking. Exp Eye Res 1999;69:1-7. https://doi.org/10.1006/exer.1999.0660
  21. Yoon HW, Chung JY, Song MS, Park H. Neural correlates of eye blinking; improved by simultaneous fMRI and EOG measurement. Neurosci Lett 2005;381:26-30. https://doi.org/10.1016/j.neulet.2005.01.077
  22. Chung JY, Yoon HW, Song MS, Park H. Event related fMRI studies of voluntary and inhibited eye blinking using a time marker of EOG. Neurosci Lett 2006;395:196-200. https://doi.org/10.1016/j.neulet.2005.10.094
  23. Kaneko K, Sakamoto K. Evaluation of three types of blinks with the use of electro-oculogram and electromyogram. Percept Mot Skills 1999;88:1037-1052. https://doi.org/10.2466/pms.1999.88.3.1037
  24. VanderWerf F, Brassinga P, Reits D, Aramideh M, Ongerboer de Visser B. Eyelid movements: behavioral studies of blinking in humans under different stimulus conditions. J Neurophysiol 2003;89:2784-2796. https://doi.org/10.1152/jn.00557.2002
  25. Irwin DE, Thomas LE. Tutorials in Visual Cognition. London: Psychology Press;2010.
  26. Bentivoglio AR, Bressman SB, Cassetta E, Carretta D, Tonali P, Albanese A. Analysis of blink rate patterns in normal subjects. Mov Disord 1997;12:1028-1034. https://doi.org/10.1002/mds.870120629
  27. Holland MK, Tarlow G. Blinking and thinking. Percept Mot Skills 1975;41:503-506.
  28. Gregory L Jr, Gregory RL. Diseases of the parathyroid glands. Tex State J Med 1952;48:741-748.
  29. Monster AW, Chan HC, O'Connor D. Long-term trends in human eye blink rate. Biotelem Patient Monit 1978;5:206-222.
  30. Schellini SA, Sampaio AA Jr, Hoyama E, Cruz AA, Padovani CR. Spontaneous eye blink analysis in the normal individual. Orbit 2005;24:239-242. https://doi.org/10.1080/01676830590922057
  31. Carney LG, Hill RM. The nature of normal blinking patterns. Acta Ophthalmol (Copenh) 1982;60:427-433.
  32. Barbato G, Ficca G, Muscettola G, Fichele M, Beatrice M, Rinaldi F. Diurnal variation in spontaneous eye-blink rate. Psychiatry Res 2000;93:145-151. https://doi.org/10.1016/S0165-1781(00)00108-6
  33. De Padova V, Barbato G, Conte F, Ficca G. Diurnal variation of spontaneous eye blink rate in the elderly and its relationships with sleepiness and arousal. Neurosci Lett 2009;463:40-43. https://doi.org/10.1016/j.neulet.2009.06.095
  34. Barbato G, De Padova V, Paolillo AR, Arpaia L, Russo E, Ficca G. Increased spontaneous eye blink rate following prolonged wakefulness. Physiol Behav 2007;90:151-154. https://doi.org/10.1016/j.physbeh.2006.09.023
  35. Orchard LN, Stern JA. Blinks as an index of cognitive activity during reading. Integr Physiol Behav Sci 1991;26:108-116. https://doi.org/10.1007/BF02691032
  36. Ichikawa N, Ohira H. Eyeblink activity as an index of cognitive processing: temporal distribution of eyeblinks as an indicator of expectancy in semantic priming. Percept Mot Skills 2004;98:131-140. https://doi.org/10.2466/pms.98.1.131-140
  37. Tada H. Spontaneous blinking during a visual tracking performance. Fukushima J Med Sci 1978;25:91-100.
  38. Fukuda K. Analysis of eyeblink activity during discriminative tasks. Percept Mot Skills 1994;79:1599-1608. https://doi.org/10.2466/pms.1994.79.3f.1599
  39. Oh J, Han M, Peterson BS, Jeong J. Spontaneous eyeblinks are correlated with response during Stroop task. PLoS One 2012 (In press).
  40. Green CS, Bavelier D. Action video game modifies visual selective attention. Nature 2003;423:534-537. https://doi.org/10.1038/nature01647
  41. Bohmelt AH, Schell AM, Dawson ME. Attentional modulation of short- and long-lead-interval modification of the acoustic startle eyeblink response: comparing auditory and visual prestimuli. Int J Psychophysiol 1999;32:239-250. https://doi.org/10.1016/S0167-8760(99)00019-7
  42. Stevens JR. Eye blink and schizophrenia: psychosis or tardive dyskinesia? Am J Psychiatry 1978;135:223-226. https://doi.org/10.1176/ajp.135.2.223
  43. Kleinman JE, Karson CN, Weinberger DR, Freed WJ, Berman KF, Wyatt RJ. Eye-blinking and cerebral ventricular size in chronic schizophrenic patients. Am J Psychiatry 1984;141:1430-1432. https://doi.org/10.1176/ajp.141.11.1430
  44. Breier A, Su TP, Saunders R, Carson RE, Kolachana BS, de Bartolomeis A, et al. Schizophrenia is associated with elevated amphetamine-induced synaptic dopamine concentrations: evidence from a novel positron emission tomography method. Proc Natl Acad Sci U S A 1997;94:2569-2574. https://doi.org/10.1073/pnas.94.6.2569
  45. Emilien G, Maloteaux JM, Geurts M, Owen MJ. Dopamine receptors and schizophrenia: contribution of molecular genetics and clinical neuropsychology. Int J Neuropsychopharmacol 1999;2:197-227. https://doi.org/10.1017/S1461145799001479
  46. Mackert A, Woyth C, Flechtner KM, Volz HP. Increased blink rate in drug-naive acute schizophrenic patients. Biol Psychiatry 1990;27:1197-1202. https://doi.org/10.1016/0006-3223(90)90417-Z
  47. Agostino R, Bologna M, Dinapoli L, Gregori B, Fabbrini G, Accornero N, et al. Voluntary, spontaneous, and reflex blinking in Parkinson's disease. Mov Disord 2008;23:669-675. https://doi.org/10.1002/mds.21887
  48. Damier P, Hirsch EC, Agid Y, Graybiel AM. The substantia nigra of the human brain. II. Patterns of loss of dopamine-containing neurons in Parkinson's disease. Brain 1999;122:1437-1448. https://doi.org/10.1093/brain/122.8.1437
  49. Tulen JH, Azzolini M, de Vries JA, Groeneveld WH, Passchier J, van De Wetering BJ. Quantitative study of spontaneous eye blinks and eye tics in Gilles de la Tourette's syndrome. J Neurol Neurosurg Psychiatry 1999;67:800-802. https://doi.org/10.1136/jnnp.67.6.800
  50. Karson CN, Kaufmann CA, Shapiro AK, Shapiro E. Eye-blink rate in Tourette's syndrome. J Nerv Ment Dis 1985;173:566-569. https://doi.org/10.1097/00005053-198509000-00008
  51. Konrad K, Gauggel S, Schurek J. Catecholamine functioning in children with traumatic brain injuries and children with attention-deficit/hyperactivity disorder. Brain Res Cogn Brain Res 2003;16:425-433. https://doi.org/10.1016/S0926-6410(03)00057-0
  52. Colzato LS, van den Wildenberg WP, Hommel B. Reduced spontaneous eye blink rates in recreational cocaine users: evidence for dopaminergic hypoactivity. PLoS One 2008;3:e3461. https://doi.org/10.1371/journal.pone.0003461
  53. Caplan R, Guthrie D, Komo S. Blink rate in children with attention-deficit- hyperactivity disorder. Biol Psychiatry 1996;39:1032-1038. https://doi.org/10.1016/0006-3223(95)00315-0
  54. Standaert DG. Update on the pathology of dystonia. Neurobiol Dis 2011;42:148-151. https://doi.org/10.1016/j.nbd.2011.01.012
  55. Tripp G, Wickens JR. Research review: dopamine transfer deficit: a neurobiological theory of altered reinforcement mechanisms in ADHD. J Child Psychol Psychiatry 2008;49:691-704. https://doi.org/10.1111/j.1469-7610.2007.01851.x
  56. Steeves TD, Ko JH, Kideckel DM, Rusjan P, Houle S, Sandor P, et al. Extrastriatal dopaminergic dysfunction in tourette syndrome. Ann Neurol 2010;67:170-181. https://doi.org/10.1002/ana.21809
  57. Holsen L, Thompson T. Compulsive behavior and eye blink in Prader-Willi syndrome: neurochemical implications. Am J Ment Retard 2004;109:197-207. https://doi.org/10.1352/0895-8017(2004)109<197:CBAEBI>2.0.CO;2
  58. Kleven MS, Koek W. Differential effects of direct and indirect dopamine agonists on eye blink rate in cynomolgus monkeys. J Pharmacol Exp Ther 1996;279:1211-1219.
  59. Taylor JR, Elsworth JD, Lawrence MS, Sladek JR Jr, Roth RH, Redmond DE Jr. Spontaneous blink rates correlate with dopamine levels in the caudate nucleus of MPTP-treated monkeys. Exp Neurol 1999;158:214-220. https://doi.org/10.1006/exnr.1999.7093
  60. Lawrence MS, Redmond DE Jr. MPTP lesions and dopaminergic drugs alter eye blink rate in African green monkeys. Pharmacol Biochem Behav 1991;38:869-874. https://doi.org/10.1016/0091-3057(91)90255-Z
  61. Elsworth JD, Lawrence MS, Roth RH, Taylor JR, Mailman RB, Nichols DE, et al. D1 and D2 dopamine receptors independently regulate spontaneous blink rate in the vervet monkey. J Pharmacol Exp Ther 1991;259:595-600.
  62. Colzato LS, van Wouwe NC, Hommel B. Spontaneous eyeblink rate predicts the strength of visuomotor binding. Neuropsychologia 2007;45:2387-2392. https://doi.org/10.1016/j.neuropsychologia.2007.03.004
  63. Gurney KN, Humphries M, Wood R, Prescott TJ, Redgrave P. Testing computational hypotheses of brain systems function: a case study with the basal ganglia. Network 2004;15:263-290. https://doi.org/10.1088/0954-898X_15_4_003
  64. Gurney K, Prescott TJ, Redgrave P. A computational model of action selection in the basal ganglia. I. A new functional anatomy. Biol Cybern 2001;84:401-410. https://doi.org/10.1007/PL00007984
  65. Colzato LS, Slagter HA, Spape MM, Hommel B. Blinks of the eye predict blinks of the mind. Neuropsychologia 2008;46:3179-3183. https://doi.org/10.1016/j.neuropsychologia.2008.07.006
  66. Sawaguchi T, Goldman-Rakic PS. D1 dopamine receptors in prefrontal cortex: involvement in working memory. Science 1991;251:947-950. https://doi.org/10.1126/science.1825731
  67. Chermahini SA, Hommel B. The (b)link between creativity and dopamine: spontaneous eye blink rates predict and dissociate divergent and convergent thinking. Cognition 2010;115:458-465. https://doi.org/10.1016/j.cognition.2010.03.007
  68. Eysenck HJ. Creativity and Personality: Suggestions for a Theory. Psychological Inquiry: An International Journal of Peer Commentary and Review 1993;4:147-217.
  69. Kulisevsky J, Pagonabarraga J, Martinez-Corral M. Changes in artistic style and behaviour in Parkinson's disease: dopamine and creativity. J Neurol 2009;256:816-819. https://doi.org/10.1007/s00415-009-5001-1
  70. Tantillo M, Kesick CM, Hynd GW, Dishman RK. The effects of exercise on children with attention-deficit hyperactivity disorder. Med Sci Sports Exerc 2002;34:203-212. https://doi.org/10.1097/00005768-200202000-00004
  71. Ramadan M, Whalen B, De Santes K. Hyperexcitable blink reflex preceding the diagnosis of neuroblastoma. J Pediatr Hematol Oncol 2004;26:665-667. https://doi.org/10.1097/01.mph.0000140657.96085.65
  72. Woodruff-Pak DS. Eyeblink classical conditioning differentiates normal aging from Alzheimer's disease. Integr Physiol Behav Sci 2001;36:87-108. https://doi.org/10.1007/BF02734044
  73. Woodruff-Pak DS, Romano S, Papka M. Training to criterion in eyeblink classical conditioning in Alzheimer's disease, Down's syndrome with Alzheimer's disease, and healthy elderly. Behav Neurosci 1996;110:22-29. https://doi.org/10.1037/0735-7044.110.1.22
  74. Woodruff-Pak DS, Papka M, Romano S, Li YT. Eyeblink classical conditioning in Alzheimer's disease and cerebrovascular dementia. Neurobiol Aging 1996;17:505-512. https://doi.org/10.1016/0197-4580(96)00070-X
  75. Woodruff-Pak DS, Papka M. Alzheimer's disease and eyeblink conditioning: 750 ms trace vs. 400 ms delay paradigm. Neurobiol Aging 1996;17:397-404. https://doi.org/10.1016/0197-4580(96)00022-X
  76. Jacobson SW, Stanton ME, Molteno CD, Burden MJ, Fuller DS, Hoyme HE, et al. Impaired eyeblink conditioning in children with fetal alcohol syndrome. Alcohol Clin Exp Res 2008;32:365-372. https://doi.org/10.1111/j.1530-0277.2007.00585.x
  77. Chen WH, Chiang TJ, Hsu MC, Liu JS. The validity of eye blink rate in Chinese adults for the diagnosis of Parkinson's disease. Clin Neurol Neurosurg 2003;105:90-92. https://doi.org/10.1016/S0303-8467(02)00107-5
  78. Biousse V, Skibell BC, Watts RL, Loupe DN, Drews-Botsch C, Newman NJ. Ophthalmologic features of Parkinson's disease. Neurology 2004;62:177-180. https://doi.org/10.1212/01.WNL.0000103444.45882.D8
  79. Armstrong RA. Visual signs and symptoms of Parkinson's disease. Clin Exp Optom 2008;91:129-138. https://doi.org/10.1111/j.1444-0938.2007.00211.x
  80. LeDoux MS, Lorden JF, Smith JM, Mays LE. Serotonergic modulation of eye blinks in cat and monkey. Neurosci Lett 1998;253:61-64. https://doi.org/10.1016/S0304-3940(98)00616-8
  81. Ursin R. Serotonin and sleep. Sleep Med Rev 2002;6:55-69. https://doi.org/10.1053/smrv.2001.0174