PUPILLOMETRY IN THE ASSESSMENT OF EMOTIONAL STATE AND COGNITIVE FUNCTIONS IN HUMAN

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

Pupillometry is a method allowing quantitative assessment of the pupil diameter. The size of the pupil is regulated by the structures of autonomic nervous system (nuclei of the oculomotor nerve, ciliospinal center) and related to the ambient lighting. However, overlying structures of the brain, in particular cortex, via locus coeruleus, upper colliculi of quadrigeminal bodies modulate the pupillary response regardless ambient lighting condition. Thus the baseline diameter of the pupil and its changes associated with certain tasks could be used for the objective assessment of the emotional state and cognitive functions in a human. There are data showing the changes in the pupillary response in patients with autism spectrum disorder, depression as well as Alzheimer’s disease, Parkinson’s disease and other organic disorders of the brain. More research in pupillometry is needed to identify new areas for its use.

About the authors

M. A. Kutlubaev

Department of Neurology Bashkir State Medical University

Author for correspondence.
Email: mansur.kutlubaev@yahoo.com
Russia, Ufa

D. R. Shagieva

Department of Neurology Bashkir State Medical University

Email: mansur.kutlubaev@yahoo.com
Russia, Ufa

G. I. Karimova

Department of Neurology Bashkir State Medical University

Email: mansur.kutlubaev@yahoo.com
Russia, Ufa

A. I. Izmalkova

Institute for Cognitive Neuroscience, National Research University Higher school of economics

Email: mansur.kutlubaev@yahoo.com
Russia, Moscow

A. V. Myachikov

Institute for Cognitive Neuroscience, National Research University Higher school of economics; Northumbria University, Newcastle upon Tyne

Email: mansur.kutlubaev@yahoo.com
Russia, Moscow; Great Britain, United Kingdom

References

  1. Барабанщиков В.А. (отв. ред.) Современная экспериментальная психология: В 2-x т., т. 1. 2011. 555 с.
  2. Barabanshchikov V.A. (ed.) Modern experimental psychology: In 2 vol., vol. 1. 2011. 555 p.
  3. Величковский Б.Б. Возможности когнитивной тренировки как метода коррекции возрастных нарушений когнитивного контроля. Экспериментальная психология. 2009. 3 (2): 78–91.
  4. Velichkovsky B.B. Performance capabilities of cognitive training as a method of correcting age-related decline in cognitive control. Experimental psychology. 2009. 3 (2): 78–91.
  5. Величковский Б.Б., Измалкова А.И. Влияние нагрузки на вербальную рабочую память при глазодвигательной активности в условиях выполнения задания зрительного поиска. Экспериментальная психология. 2015. 2 (8): 21–35.
  6. Velichkovsky B.B., Izmalkova A.I. Effect of verbal working memory load on eye movements in visual search. Experimental Psychology. 2015. 2 (8): 21–35.
  7. Горюшко С.М., Самочадин А.В. Средства оценки уровня когнитивной нагрузки в процессе обучения. Компьютерные инструменты в образовании. 2018. 4: 35–44. doi:
  8. Goryushko S.M., Samochadin A.V. Tools for Cognitive Load Evaluation in the Education Process. Computer tools in education, no. 4, pp. 35–44, 2018 (in Russian). https://doi.org/10.32603/2071-2340-4-35-44
  9. Девятко И.Ф., Богданов М.Б., Лебедев Д.В. Динамика диаметра зрачка как индикатор когнитивной нагрузки респондента: методический эксперимент по сравнению CASI и P&PSI вопросников. Вестник Российского университета дружбы народов. Серия: Социология. 2021. 21 (1): 36–49. https://doi.org/10.22363/2313-2272-2021-21-1-36-49
  10. Deviatko I.F., Bogdanov M.B., Lebedev D.V. Pupil diameter dynamics as an indicator of the respondent’s cognitive load: Methodological experiment comparing CASI and P&PSI // RUDN J. Sociology. 2021. 21 (1): 36–49. https://doi.org/10.22363/2313-2272-2021-21-1-36-49
  11. Куцало А.Л., Цимбал М.В., Штейнберг Н.В., Хомич Д.С., Вареников М.Г., Волков В.В. Особенности бинокулярной динамической пупиллометрии у больных сахарным диабетом II типа. Практическая медицина. 2018. 16 (5): 162–167 https://doi.org/10.32000/2072-1757-2018-16-5-162-167
  12. Kutsalo A.L, Tsimbal M.V., Shtejnberg N.V., Khomich D.S., Varenikov M.G., Volkov V.V. Features of binocular dynamic pupillometry in patients with type 2 diabetes mellitus. Practical Medicine. 2018. 16 (5): 162–167 https://doi.org/10.32000/2072-1757-2018-16-5-162-167
  13. Ошоров А.В., Александрова Е.В., Мурадян К.Р., Сосновская О.Ю., Соколова Е.Ю., Савин И.А. Пупиллометрия как метод мониторинга фотореакции в нейрореанимации. Журн. “Вопросы нейрохирургии” имени Н.Н. Бурденко. 2021. 85 (3): 117 123. https://doi.org/10.17116/neiro202185031117
  14. Oshorov A.V., Aleksandrova E.V., Muradyan K.R., Sosnovskaya O.Yu., Sokolova E.Yu., Savin I.A. Pupillometry as a method for monitoring of pupillary light reflex in ICU patients. Zhurnal Voprosy Neirokhirurgii Imeni N.N. Burdenko. 2021. 85 (3): 117 123. (In Russ., In Engl.). https://doi.org/10.17116/neiro202185031117
  15. Походай М.Ю., Бермудес-Маргаретто Б., Штыров Ю.Ю., Мячиков А.В. Методика айтрекинга в психолингвистике и паралелльная регистрация с ЭЭГ. Журн. высшей нервной деятельности им. И.П. Павлова. 2022. 72 (5): 609–622. https://doi.org/10.31857/S0044467722050124
  16. Pokhoday M., Bermudez-Margaretto B., Shtyrov Y., Myachykov A. Eye tracking application in psycholinguistic and parallel registration with EEG. Zhurnal Vysshei Nervnoi Deyatelnosti Imeni I.P. Pavlovathis link is disabled. 2022. 72 (5): 609–622. https://doi.org/10.31857/S0044467722050124
  17. Пучкова А.Н., Ткаченко О.Н., Дорохов В.Б. Специфика динамики размера зрачка в процессе работы с арифметическими задачами. Социально-экологические технологии. 2017. 3: 80–91.
  18. Puchkova A.N., Tkachenko O.N., Dorohov V.B. Specifics of pupil size dynamics in the process of working with arithmetic tasks. Environment and Human: Ecological Studies. 2017. 3: 80–91.
  19. Романова Н.М., Рытик А.П., Самохина М.А., Скрипаль А.В., Усанов Д.А. Особенности глазодвигательных реакций человека при произнесении истинной и ложной информации. Известия Саратовского университета. Новая серия. Серия Философия. Психология. Педагогика. 2008. 8 (1): 65–73.
  20. Romanova N.M., Rytik A.P., Samokhina M.A., Skripal A.V., Usanov D.A. The Peculiarities of Oculomotor Reactions of a Person Telling False or True Information. Izvestiya of Saratov University. Philosophy. Psychology. Pedagogy. 2008. 8 (1): 65–73.
  21. Саховская Н.А., Фролов М.А., Казакова К.А., Колодкина М.Г. История развития пупиллографии и возможности ее применения в современной офтальмологии. Офтальмология. 2022. 19 (3): 475–481. https://doi.org/10.18008/1816-5095-2022-3-475-481
  22. Sakhovskaya N.A., Frolov M.A., Kazakova K.A., Kolodkina M.G. The History of Pupillography and Possibility of Its Using in Modern Ophthalmology. Ophthalmology in Russia. 2022. 19 (3): 475–481. (In Russ.) https://doi.org/10.18008/1816-5095-2022-3-475-481
  23. Aguillon-Hernandez N., Mofid Y, Latinus M., Roché L., Bufo M.R., Lemaire M., Malvy J., Martineau J., Wardak C., Bonnet-Brilhault F. The pupil: a window on social automatic processing in autism spectrum disorder children. J. Child Psychol Psychiatry. 2020. 61 (7): 768–778. https://doi.org/10.1111/jcpp.13170
  24. Alhassan M., Hovis J.K., Almeida Q.J. Pupil light reflex in Parkinson’s disease patients with and without freezing of gait symptoms. Saudi J. Ophthalmol. 2022. 35 (4): 332–340. https://doi.org/10.4103/1319-4534.347306
  25. Aminihajibashi S., Hagen T., Foldal M.D., Laeng B., Espeseth T. Individual differences in resting-state pupil size: Evidence for association between working memory capacity and pupil size variability. Int. J. Psychophysiol. 2019. 140: 1–7. https://doi.org/10.1016/j.ijpsycho.2019.03.007
  26. Anderson C.J., Colombo J. Larger tonic pupil size in young children with autism spectrum disorder. Dev. Psychobiol. 2009. 51 (2): 207–11. https://doi.org/10.1002/dev.20352
  27. Aston-Jones G., Cohen J.D. An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu Rev Neurosci. 2005. 28: 403–50. https://doi.org/10.1146/annurev.neuro.28.061604.135709
  28. Beissner F., Meissner K., Bär K.J., Napadow V. The autonomic brain: an activation likelihood estimation meta-analysis for central processing of autonomic function. J. Neurosci. 2013. 33 (25): 10503-11. https://doi.org/10.1523/JNEUROSCI.1103-13.2013
  29. Benarroch E. What Are Current Concepts on the Functional Organization of the Locus Coeruleus and Its Role in Cognition and Neurodegeneration? Neurology. 2023. 100 (3): 132–137. https://doi.org/10.1212/WNL.0000000000206736
  30. Bouma H., Baghuis L.C.J. Hippus of the pupil: periods of slow oscillations of unknown origin. Vision Research. 1971. 11 (11): 1345–1351. https://doi.org/10.1016/0042-6989(71)90016-2
  31. Bower M.M., Sweidan A.J., Xu J.C., Stern-Neze S, Yu W., Groysman L.I. Quantitative Pupillometry in the Intensive Care Unit. J. Intensive Care Med. 2021. 36 (4): 383–391. doi: 10.1177/0885066619881124. Epub 2019 Oct 10. PMID: 31601157.
  32. Bradley M.M., Sapigao R.G., Lang P.J. Sympathetic ANS modulation of pupil diameter in emotional scene perception: Effects of hedonic content, brightness, and contrast. Psychophysiology. 2017. 54 (10): 1419–1435. https://doi.org/10.1111/psyp.12890
  33. Brown V.A., McLaughlin D.J., Strand J.F., Van Engen K.J. Rapid adaptation to fully intelligible nonnative-accented speech reduces listening effort. Quarterly J. Experimental Psychology. 2020. 73 (9): 1431–1443. https://doi.org/10.1177/1747021820916726
  34. Bufo M.R., Guidotti M., De Faria C., Mofid Y., Bonnet-Brilhault F., Wardak C., Aguillon-Hernandez N. Autonomic tone in children and adults: Pupillary, electrodermal and cardiac activity at rest. Int. J. Psychophysiol. 2022. 180: 68–78. https://doi.org/10.1016/j.ijpsycho.2022.07.009
  35. Burkhouse K.L., Siegle G.J., Gibb B.E. Pupillary reactivity to emotional stimuli in children of depressed and anxious mothers. J. Child Psychol Psychiatry. 2014. 55 (9): 1009-16. https://doi.org/10.1111/jcpp.12225
  36. Chougule P.S., Najjar R.P., Finkelstein M.T., Kandiah N., Milea D. Light-Induced Pupillary Responses in Alzheimer’s Disease. Front Neurol. 2019. 10: 360. https://doi.org/10.3389/fneur.2019.00360
  37. Cohen J.R., Thakur H., Burkhouse K.L., Gibb B.E. A multimethod screening approach for pediatric depression onset: An incremental validity study. J. Consult Clin Psychol. 2019. 87 (2): 184–197. https://doi.org/10.1037/ccp0000364
  38. Czerniak J.N., Schierhorst N., Brandl C., Mertens A., Schwalm M., Nitsch V. A meta-analytic review of the reliability of the Index of Cognitive Activity concerning task-evoked cognitive workload and light influences. Acta Psychol (Amst). 2021. 220: 103402. https://doi.org/10.1016/j.actpsy.2021.103402
  39. de Vries L., Fouquaet I., Boets B., Naulaers G., Steyaert J. Autism spectrum disorder and pupillometry: A systematic review and meta-analysis. Neurosci Biobehav Rev. 2021. 120: 479–508. https://doi.org/10.1016/j.neubiorev.2020.09.032
  40. Daniel M., Charier D., Pereira B., Pachcinski M., Sharshar T., Molliex S. Prognosis value of pupillometry in COVID-19 patients admitted in intensive care unit. Auton Neurosci. 2022. 245: 103057. https://doi.org/10.1016/j.autneu.2022.103057
  41. de Rodez Benavent S.A, Nygaard G.O., Harbo H.F., Tønnesen S., Sowa P., Landrø N.I., Wendel-Haga M., Etholm L., Nilsen K.B., Drolsum L., Kerty E., Celius E.G., Laeng B. Fatigue and cognition: Pupillary responses to problem-solving in early multiple sclerosis patients. Brain Behav. 2017. 7 (7): e00717. https://doi.org/10.1002/brb3.717
  42. De Zorzi L., Ranfaing S., Honoré J., Sequeira H. Autonomic reactivity to emotion: A marker of sub-clinical anxiety and depression symptoms? Psychophysiology. 2021. 58 (4): e13774. https://doi.org/10.1111/psyp.13774
  43. DiCriscio A.S., Troiani V. Pupil adaptation corresponds to quantitative measures of autism traits in children. Sci. Rep. 2017. 7 (1): 6476. https://doi.org/10.1038/s41598-017-06829-1
  44. DiNuzzo M., Mascali D., Moraschi M., Bussu G., Maugeri L., Mangini F., Fratini M., Giove F. Brain Networks Underlying Eye’s Pupil Dynamics. Front Neurosci. 2019. 13: 965. https://doi.org/10.3389/fnins.2019.00965
  45. Douglas V.P., Douglas K.A.A., Cestari D.M. Ophthalmic manifestations of dementing disorders. Curr Opin Ophthalmol. 2021. 32 (6): 515–520. https://doi.org/10.1097/ICU.0000000000000807
  46. Ebitz R.B., Moore T. Selective Modulation of the Pupil Light Reflex by Microstimulation of Prefrontal Cortex. J. Neurosci. 2017. 37 (19): 5008–5018. https://doi.org/10.1523/JNEUROSCI.2433-16.2017
  47. El Haj M., Chapelet G., Moustafa A.A., Boutoleau-Bretonnière C. Pupil size as an indicator of cognitive activity in mild Alzheimer’s disease. EXCLI J. 2022. 21: 307–316. https://doi.org/10.17179/excli2021-4568
  48. Fan X., Miles J.H., Takahashi N., Yao G. Abnormal transient pupillary light reflex in individuals with autism spectrum disorders. J. Autism Dev. Disord. 2009. 39 (11): 1499–508. https://doi.org/10.1007/s10803-009-0767-7
  49. Fattal J., Brascamp J.W., Slate R.E., Lehet M., Achtyes E.D., Thakkar K.N. Blunted pupil light reflex is associated with negative symptoms and working memory in individuals with schizophrenia. Schizophr Res. 2022. 248: 254–262. Epub 2022 Sep 14.https://doi.org/10.1016/j.schres.2022.09.019
  50. Ferencová N., Višňovcová Z., Bona Olexová L., Tonhajzerová I. Eye pupil – a window into central autonomic regulation via emotional/cognitive processing. Physiol Res. 2021. 70(Suppl4): S669–S682. https://doi.org/10.33549/physiolres.934749
  51. Guath M., Willfors C., Björlin Avdic H., Nordgren A., Kleberg J.L. Pupillary response in reward processing in adults with major depressive disorder in remission. J. Int. Neuropsychol. Soc. 2022 May. 12: 1–10. https://doi.org/10.1017/S1355617722000224
  52. Gusso M.M., Serur G., Nohama P. Pupil Reactions to Tactile Stimulation: A Systematic Review. Front Neurosci. 2021. 15: 610841. https://doi.org/10.3389/fnins.2021.610841
  53. Joshi S., Gold J.I. Pupil Size as a Window on Neural Substrates of Cognition. Trends Cogn Sci. 2020. 24 (6): 466–480. https://doi.org/10.1016/j.tics.2020.03.005
  54. Joshi S., Li Y., Kalwani R.M., Gold J.I. Relationships between Pupil Diameter and Neuronal Activity in the Locus Coeruleus, Colliculi, and Cingulate Cortex. Neuron. 2016. 89 (1): 221–34. https://doi.org/10.1016/j.neuron.2015.11.028
  55. Henderson R.R., Bradley M.M., Lang P.J. Modulation of the initial light reflex during affective picture viewing. Psychophysiology. 2014. 51 (9): 815–8. https://doi.org/10.1111/psyp.12236
  56. Keil V., Hepach R., Vierrath S., Caffier D., Tuschen-Caffier B., Klein C., Schmitz J. Children with social anxiety disorder show blunted pupillary reactivity and altered eye contact processing in response to emotional faces: Insights from pupillometry and eye movements. J. Anxiety Disord. 2018. 58: 61–69. https://doi.org/10.1016/j.janxdis.2018.07.001
  57. Kleberg J.L., Hanqvist C., Serlachius E., Högström J. Pupil dilation to emotional expressions in adolescent social anxiety disorder is related to treatment outcome. J Anxiety Disord. 2019. 65: 26–33. https://doi.org/10.1016/j.janxdis.2019.04.006
  58. Kumano H., Nobukawa S., Shirama A., Takahashi T., Takeda T., Ohta H., Kikuchi M., Iwanami A., Kato N., Toda S. Asymmetric Complexity in a Pupil Control Model With Laterally Imbalanced Neural Activity in the Locus Coeruleus: A Potential Biomarker for Attention-Deficit/Hyperactivity Disorder. Neural Comput. 2022. 34 (12): 2388–2407. PMID: 3623044.
  59. Laeng B., Ørbo M., Holmlund T., Miozzo M. Pupillary Stroop effects. Cognitive Processing. 2011. 12 (1): 13–21. https://doi.org/10.1007/s10339-010-0370-z
  60. Lawson R.P., Mathys C., Rees G. Adults with autism overestimate the volatility of the sensory environment. Nat Neurosci. 2017. 20 (9): 1293–1299. https://doi.org/10.1038/nn.4615
  61. Lustig-Barzelay Y., Sher I., Sharvit-Ginon I., Feldman Y., Mrejen M., Dallasheh S., Livny A., Schnaider Beeri M., Weller A., Ravona-Springer R., Rotenstreich Y. Machine learning for comprehensive prediction of high risk for Alzheimer’s disease based on chromatic pupilloperimetry. Sci. Rep. 2022. 12 (1): 9945. https://doi.org/10.1038/s41598-022-13999-0
  62. Mäki-Marttunen V. Pupil-based States of Brain Integration across Cognitive States. Neuroscience. 2021. 471: 61–71. Epub 2021 Jul 23.https://doi.org/10.1016/j.neuroscience.2021.07.016
  63. Martineau J., Hernandez N., Hiebel L., Roché L., Metzger A., Bonnet-Brilhault F. Can pupil size and pupil responses during visual scanning contribute to the diagnosis of autism spectrum disorder in children? J. Psychiatr Res. 2011. 45 (8): 1077–82. https://doi.org/10.1016/j.jpsychires.2011.01.008
  64. Marzouki Y., Dusaucy V., Chanceaux M., Mathôt S. The World (of Warcraft) through the eyes of an expert. PeerJ. 2017. 5: e3783. https://doi.org/10.7717/peerj.3783
  65. Mathôt S. Pupillometry: Psychology, Physiology, and Function. J. Cogn. 2018. 1 (1): 16. https://doi.org/10.5334/joc.18
  66. McKendrick R., Harwood A. Cognitive Workload and Workload Transitions Elicit Curvilinear Hemodynamics During Spatial Working Memory. Front Hum Neurosci. 2019. 13: 405. https://doi.org/10.3389/fnhum.2019.00405
  67. Mestanikova A., Ondrejka I., Mestanik M., Cesnekova D., Visnovcova Z., Bujnakova I., Oppa M., Calkovska A., Tonhajzerova I. Pupillary light reflex is altered in adolescent depression. Physiol Res. 2017. 66 (Suppl 2): S277–S284. https://doi.org/10.33549/physiolres.933683
  68. Miller A.L., Gross M.P., Unsworth N. Individual differences in working memory capacity and long-term memory: The influence of intensity of attention to items at encoding as measured by pupil dilation. J. Memory and Language. 2019. 104: 25–42. https://doi.org/10.1016/j.jml.2018.09.005
  69. Morad Y., Lemberg H., Yofe N., Dagan Y. Pupillography as an objective indicator of fatigue. Current Eye Research. 2000. 21 (1): 535–542. https://doi.org/10.1076/0271-3683(200007)2111-ZFT535
  70. Oh A.J., Amore G., Sultan W., Asanad S., Park J.C., Romagnoli M., La Morgia C., Karanjia R., Harrington M.G., Sadun A.A. Pupillometry evaluation of melanopsin retinal ganglion cell function and sleep-wake activity in pre-symptomatic Alzheimer’s disease. PLoS One. 2019. 14 (12): e0226197. Erratum in: PLoS One. 2020 Feb 27. 15 (2): e0230061.https://doi.org/10.1371/journal.pone.0226197
  71. Park K.W., Choi N., Ryu H.S., Kim M.S., Lee E.J., Chung S.J. Pupillary dysfunction of multiple system atrophy: Dynamic pupillometric findings and clinical correlations. Parkinsonism Relat Disord. 2019. 65: 234–237. https://doi.org/10.1016/j.parkreldis.2019.05.003
  72. Peinkhofer C., Knudsen G.M., Moretti R., Kondziella D. Cortical modulation of pupillary function: systematic review. PeerJ. 2019. 7: e6882. https://doi.org/10.7717/peerj.6882
  73. Portugal A.M., Taylor M.J., Viktorsson C., Nyström P., Li D., Tammimies K., Ronald A., Falck-Ytter T. Pupil size and pupillary light reflex in early infancy: heritability and link to genetic liability to schizophrenia. J Child Psychol Psychiatry. 2022. 63 (9): 1068–1077. Epub 2021 Dec 23.https://doi.org/10.1111/jcpp.13564
  74. Posner M.I., Snyder C.R., Solso R. Attention and cognitive control. Cognitive psychology: Key readings. 2004. 205: 55–85.
  75. Price R.B., Rosen D., Siegle G.J., Ladouceur C.D., Tang K., Allen K.B., Ryan N.D., Dahl R.E., Forbes E.E., Silk J.S. From anxious youth to depressed adolescents: Prospective prediction of 2-year depression symptoms via attentional bias measures. J. Abnorm Psychol. 2016 Feb. 125 (2): 267–278. https://doi.org/10.1037/abn0000127
  76. Quadt L., Critchley H., Nagai Y. Cognition, emotion, and the central autonomic network. Auton Neurosci. 2022. 238: 102948. doi: 10.1016/j.autneu.2022.102948. Epub ahead of print. PMID: 35149372.
  77. Richardson D.C., Dale R., Spivey M.J. Eye movements in language and cognition. Methods in cognitive linguistics. 2007. 18: 323–344.
  78. Robison M.K., Coyne J.T., Sibley C., Brown N.L., Neilson B., Foroughi C. An examination of relations between baseline pupil measures and cognitive abilities. Psychophysiology. 2022. 59 (12): e14124. https://doi.org/10.1111/psyp.14124
  79. Romagnoli M., Stanzani Maserati M., De Matteis M., Capellari S., Carbonelli M., Amore G., Cantalupo G., Zenesini C., Liguori R., Sadun A.A., Carelli V., Park J.C., La Morgia C. Chromatic Pupillometry Findings in Alzheimer’s Disease. Front Neurosci. 2020. 14: 780. https://doi.org/10.3389/fnins.2020.00780
  80. Rondeel E.W., van Steenbergen H., Holland R.W., van Knippenberg A. A closer look at cognitive control: differences in resource allocation during updating, inhibition and switching as revealed by pupillometry. Front Hum Neurosci. 2015. 9: 494. https://doi.org/10.3389/fnhum.2015.00494
  81. Siegle G.J., Steinhauer S.R., Carter C.S., Ramel W., Thase M.E. Do the Seconds Turn Into Hours? Relationships between Sustained Pupil Dilation in Response to Emotional Information and Self-Reported Rumination. Cognitive Therapy and Research. 2003. 27: 365–382. https://doi.org/10.1023/A:1023974602357
  82. Schneider M., Hathway P., Leuchs L., Sämann P.G., Czisch M., Spoormaker V.I. Spontaneous pupil dilations during the resting state are associated with activation of the salience network. Neuroimage. 2016. 139: 189–201. https://doi.org/10.1016/j.neuroimage.2016.06.011
  83. Shic F., Naples A.J., Barney E.C., Chang S.A., Li B., McAllister T., Kim M., Dommer K.J., Hasselmo S., Atyabi A., Wang Q., Helleman G., Levin A.R., Seow H., Bernier R., Charwaska K., Dawson G., Dziura J., Faja S., Jeste S.S., Johnson S.P., Murias M., Nelson C.A., Sabatos-DeVito M., Senturk D., Sugar C.A., Webb S.J., McPartland J.C. The autism biomarkers consortium for clinical trials: evaluation of a battery of candidate eye-tracking biomarkers for use in autism clinical trials. Mol Autism. 2022. 13 (1): 15. https://doi.org/10.1186/s13229-021-00482-2
  84. Skaramagkas V., Giannakakis G., Ktistakis E., Manousos D., Karatzanis I., Tachos N., Tripoliti E.E., Marias K., Fotiadis D.I., Tsiknakis M. Review of eye tracking metrics involved in emotional and cognitive processes. IEEE Rev Biomed Eng. 2021. PP. https://doi.org/10.1109/RBME.2021.3066072
  85. Sklerov M., Dayan E., Browner N. Functional neuroimaging of the central autonomic network: recent developments and clinical implications. Clin Auton Res. 2019. 29 (6): 555–566. Epub 2018 Nov 23.https://doi.org/10.1007/s10286-018-0577-0
  86. Sperandio I., Bond N., Binda P. Pupil Size as a Gateway Into Conscious Interpretation of Brightness. Front Neurol. 2018. 9: 1070. https://doi.org/10.3389/fneur.2018.01070
  87. Steinhauer S.R., Siegle G.J., Condray R., Pless M. Sympathetic and parasympathetic innervation of pupillary dilation during sustained processing. Int. J. Psychophysiol. 2004. 52 (1): 77–86. https://doi.org/10.1016/j.ijpsycho.2003.12.005
  88. Strauch C., Wang C.A., Einhäuser W., Van der Stigchel S., Naber M. Pupillometry as an integrated readout of distinct attentional networks. Trends Neurosci. 2022. 45 (8): 635–647. https://doi.org/10.1016/j.tins.2022.05.003
  89. Sulutvedt U., Mannix T.K., Laeng B. Gaze and the Eye Pupil Adjust to Imagined Size and Distance. Cogn Sci. 2018. 42 (8): 3159–3176. https://doi.org/10.1111/cogs.12684
  90. Sweller J. Element interactivity and intrinsic, extraneous, and germane cognitive load. Educational psychology review. 2010. 22 (2): 123–138. https://doi.org/10.1007/s10648-010-9128-510
  91. Sweller J. Cognitive load during problem solving: Effects on learning. Cognitive science. 1988. 12 (2): 257–285. https://doi.org/10.1016/0364-0213(88)90023-7
  92. Szabadi E. Functional neuroanatomy of the central noradrenergic system. J Psychopharmacol. 2013. 27 (8): 659–93. Epub 2013 Jun 12. Erratum in: J. Psychopharmacol. 2013 Oct. 27 (10): 964.https://doi.org/10.1177/0269881113490326
  93. Tsitsi P., Benfatto M.N., Seimyr G.Ö., Larsson O., Svenningsson P., Markaki I. Fixation Duration and Pupil Size as Diagnostic Tools in Parkinson’s Disease. J. Parkinsons Dis. 2021. 11 (2): 865–875. https://doi.org/10.3233/JPD-202427
  94. Tsukahara J.S., Engle R.W. Is baseline pupil size related to cognitive ability? Yes (under proper lighting conditions). Cognition. 2021. 211: 104643. https://doi.org/10.1016/j.cognition.2021.104643
  95. Turnbull P.R., Irani N., Lim N., Phillips J.R. Origins of Pupillary Hippus in the Autonomic Nervous System. Invest Ophthalmol Vis Sci. 2017. 58 (1): 197–203. https://doi.org/10.1167/iovs.16-20785
  96. Van Engen K.J., McLaughlin D.J. Eyes and ears: Using eye tracking and pupillometry to understand challenges to speech recognition. Hearing Research. 2018. 369: 56–66.
  97. Van Gerven P., Paas F., Van Merrienboer J., Schmidt H. Memory load and the cognitive pupillary response in aging. Psychophysiology. 2014. 41 (2): 167–174. https://doi.org/10.1111/j.1469-8986.2003.00148.x
  98. Viglione A., Mazziotti R., Pizzorusso T. From pupil to the brain: New insights for studying cortical plasticity through pupillometry. Front Neural Circuits. 2023. 17: 1151847. PMID: 37063384; PMCID: PMC10102476.https://doi.org/10.3389/fncir.2023.115184737063384
  99. Vogels J., Demberg V., Kray J. The Index of Cognitive Activity as a Measure of Cognitive Processing Load in Dual Task Settings. Front Psychol. 2018. 9: 2276. https://doi.org/10.3389/fpsyg.2018.02276
  100. Wang C.A., Boehnke S.E., Itti L., Munoz D.P. Transient pupil response is modulated by contrast-based saliency. J. Neurosci. 2014. 34 (2): 408–17. https://doi.org/10.1523/JNEUROSCI.3550-13.2014
  101. Wang C.A., Munoz D.P. A circuit for pupil orienting responses: implications for cognitive modulation of pupil size. Curr Opin Neurobiol. 2015. 33: 134–40. https://doi.org/10.1016/j.conb.2015.03.018
  102. Wanyan X., Zhuang D., Zhang H. Improving pilot mental workload evaluation with combined measures. Biomed Mater Eng. 2014. 24 (6): 2283–90. https://doi.org/10.3233/BME-141041
  103. Wierwille W.W., Eggemeier F.T. Recommendations for Mental Workload Measurement in a Test and Evaluation Environment. Human Factors. 1993. 35 (2): 263–281. https://doi.org/10.1177/001872089303500205
  104. White O., French R.M. Pupil Diameter May Reflect Motor Control and Learning. J. Mot. Behav. 2017. 49 (2): 141–149. https://doi.org/10.1080/00222895.2016.1161593
  105. Wu F., Zhao Y., Zhang H. Ocular Autonomic Nervous System: An Update from Anatomy to Physiological Functions. Vision (Basel). 2022. 6 (1): 6. https://doi.org/10.3390/vision6010006
  106. Yeung M.K., Lee T.L., Han Y.M.Y., Chan A.S. Prefrontal activation and pupil dilation during n-back task performance: A combined fNIRS and pupillometry study. Neuropsychologia, 2021. 159: 107954. https://doi.org/10.1016/j.neuropsychologia.2021.10-7954
  107. Yokoi A., Weiler J. Pupil diameter tracked during motor adaptation in humans. J. Neurophysiol. 2022. 128 (5): 1224–1243. https://doi.org/10.1152/jn.00021.2022
  108. You S., Hong J.H., Yoo J. Analysis of pupillometer results according to disease stage in patients with Parkinson’s disease. Sci Rep. 2021. 11 (1): 17880. https://doi.org/10.1038/s41598-021-97599-4

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2.

Download (86KB)
Indexing metadata

Copyright (c) 2023 М.А. Кутлубаев, Д.Р. Шагиева, Г.И. Каримова, А.И. Измалкова, А.В. Мячиков

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies