Skip to main content
Top
Published in: BMC Medical Informatics and Decision Making 1/2016

Open Access 01-12-2016 | Research article

Pupil diameter changes reflect difficulty and diagnostic accuracy during medical image interpretation

Authors: Tad T. Brunyé, Marianna D. Eddy, Ezgi Mercan, Kimberly H. Allison, Donald L. Weaver, Joann G. Elmore

Published in: BMC Medical Informatics and Decision Making | Issue 1/2016

Login to get access

Abstract

Background

No automated methods exist to objectively monitor and evaluate the diagnostic process while physicians review computerized medical images. The present study tested whether using eye tracking to monitor tonic and phasic pupil dynamics may prove valuable in tracking interpretive difficulty and predicting diagnostic accuracy.

Methods

Pathologists interpreted digitized breast biopsies varying in diagnosis and rated difficulty, while pupil diameter was monitored. Tonic diameter was recorded during the entire duration of interpretation, and phasic diameter was examined when the eyes fixated on a pre-determined diagnostic region during inspection.

Results

Tonic pupil diameter was higher with increasing rated difficulty levels of cases. Phasic diameter was interactively influenced by case difficulty and the eventual agreement with consensus diagnosis. More difficult cases produced increases in pupil diameter, but only when the pathologists’ diagnoses were ultimately correct. All results were robust after adjusting for the potential impact of screen brightness on pupil diameter.

Conclusions

Results contribute new understandings of the diagnostic process, theoretical positions regarding locus coeruleus-norepinephrine system function, and suggest novel approaches to monitoring, evaluating, and guiding medical image interpretation.
Literature
1.
go back to reference Krupinski EA, Tillack AA, Richter L, Henderson J, Bhattacharyya AK, Scott KM, Graham AR, Descour MR, Davis JR, Weinstein RS. Implications for medical education and differences with experience. Hum Pathol. 2006;37:1543–56. Krupinski EA, Tillack AA, Richter L, Henderson J, Bhattacharyya AK, Scott KM, Graham AR, Descour MR, Davis JR, Weinstein RS. Implications for medical education and differences with experience. Hum Pathol. 2006;37:1543–56.
2.
go back to reference Kundel HL, La Follette PS. Visual search patterns and experience with radiological images. Radiology. 1972;103:523–8.CrossRefPubMed Kundel HL, La Follette PS. Visual search patterns and experience with radiological images. Radiology. 1972;103:523–8.CrossRefPubMed
3.
go back to reference Brunyé TT, Carney PA, Allison KH, Shapiro LG, Weaver DL, Elmore JG. Eye movements as an index of pathologist visual expertise: a pilot study. PLoS One. 2014;9, e103447.CrossRefPubMedPubMedCentral Brunyé TT, Carney PA, Allison KH, Shapiro LG, Weaver DL, Elmore JG. Eye movements as an index of pathologist visual expertise: a pilot study. PLoS One. 2014;9, e103447.CrossRefPubMedPubMedCentral
4.
go back to reference Gilzenrat MS, Nieuwenhuis S, Jepma M, Cohen JD. Pupil diameter tracks changes in control state predicted by the adaptive gain theory of locus coeruleus function. Cogn Affect Behav Neurosci. 2010;10:252–69.CrossRefPubMedPubMedCentral Gilzenrat MS, Nieuwenhuis S, Jepma M, Cohen JD. Pupil diameter tracks changes in control state predicted by the adaptive gain theory of locus coeruleus function. Cogn Affect Behav Neurosci. 2010;10:252–69.CrossRefPubMedPubMedCentral
5.
go back to reference Aston-Jones G, Cohen JD. An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu Rev Neurosci. 2005;28:403–50.CrossRefPubMed Aston-Jones G, Cohen JD. An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu Rev Neurosci. 2005;28:403–50.CrossRefPubMed
6.
go back to reference Usher M, Cohen JD, Servan-Schrieber D, Rajkowski J, Aston-Jones G. The Role of Locus Coeruleus in the Regulation of Cognitive Performance. Science. 1999;283:549–54.CrossRefPubMed Usher M, Cohen JD, Servan-Schrieber D, Rajkowski J, Aston-Jones G. The Role of Locus Coeruleus in the Regulation of Cognitive Performance. Science. 1999;283:549–54.CrossRefPubMed
7.
go back to reference Laeng B, Sirois S, Gredeback G. Pupillometry: a window to the preconscious? Perspect Psychol Sci. 2012;7:18–27.CrossRefPubMed Laeng B, Sirois S, Gredeback G. Pupillometry: a window to the preconscious? Perspect Psychol Sci. 2012;7:18–27.CrossRefPubMed
8.
go back to reference Beatty J. Task-evoked pupillary responses, processing load, and the structure of processing resources. Psychol Bull. 1982;91:276–92.CrossRefPubMed Beatty J. Task-evoked pupillary responses, processing load, and the structure of processing resources. Psychol Bull. 1982;91:276–92.CrossRefPubMed
9.
go back to reference Privitera CM, Renninger LW, Carney T, Klein S, Aguilar M. Pupil dilation during visual target detection. J Vis. 2010;10:3.CrossRefPubMed Privitera CM, Renninger LW, Carney T, Klein S, Aguilar M. Pupil dilation during visual target detection. J Vis. 2010;10:3.CrossRefPubMed
10.
go back to reference Einhäuser W, Stout J, Koch C, Carter O. Pupil dilation reflects perceptual selection and predicts subsequent stability in perceptual rivalry. Proc Natl Acad Sci U S A. 2008;105:1704–9.CrossRefPubMedPubMedCentral Einhäuser W, Stout J, Koch C, Carter O. Pupil dilation reflects perceptual selection and predicts subsequent stability in perceptual rivalry. Proc Natl Acad Sci U S A. 2008;105:1704–9.CrossRefPubMedPubMedCentral
11.
go back to reference Rajkowski J, Kubiak P, Aston-Jones G. Locus coeruleus activity in monkey: phasic and tonic changes are associated with altered vigilance. Brain Res Bull Vol. 1994;35:607–16.CrossRef Rajkowski J, Kubiak P, Aston-Jones G. Locus coeruleus activity in monkey: phasic and tonic changes are associated with altered vigilance. Brain Res Bull Vol. 1994;35:607–16.CrossRef
12.
go back to reference Aston-Jones G, Rajkowski J, Kubiak P, Alexinsky T. Locus coeruleus neurons in monkey are selectively activated by attended cues in a vigilance task. J Neurosci. 1994;14:4467–80.PubMed Aston-Jones G, Rajkowski J, Kubiak P, Alexinsky T. Locus coeruleus neurons in monkey are selectively activated by attended cues in a vigilance task. J Neurosci. 1994;14:4467–80.PubMed
13.
go back to reference Schulz CM, Schneider E, Fritz L, Vockeroth J, Hapfelmeier A, Wasmaier M, Kochs EF, Schneider G. Eye tracking for assessment of workload: a pilot study in an anaesthesia simulator environment. Br J Anaesth. 2011;106:44–50. Schulz CM, Schneider E, Fritz L, Vockeroth J, Hapfelmeier A, Wasmaier M, Kochs EF, Schneider G. Eye tracking for assessment of workload: a pilot study in an anaesthesia simulator environment. Br J Anaesth. 2011;106:44–50.
14.
go back to reference Zheng B, Jiang X, Atkins MS. Detection of changes in surgical difficulty: evidence from pupil responses. Surg Innov. 2015;22:629–35.CrossRefPubMed Zheng B, Jiang X, Atkins MS. Detection of changes in surgical difficulty: evidence from pupil responses. Surg Innov. 2015;22:629–35.CrossRefPubMed
15.
go back to reference Richstone L, Schwartz MJ, Seideman C, Cadeddu J, Marshall S, Kavoussi LR. Eye metrics as an objective assessment of surgical skill. Ann Surg. 2010;252:177–82.CrossRefPubMed Richstone L, Schwartz MJ, Seideman C, Cadeddu J, Marshall S, Kavoussi LR. Eye metrics as an objective assessment of surgical skill. Ann Surg. 2010;252:177–82.CrossRefPubMed
16.
go back to reference Szulewski A, Roth N, Howes D. The use of task-evoked pupillary response as an objective measure of cognitive load in novices and trained physicians: a new tool for the assessment of expertise. Acad Med. 2015;90:981–7.CrossRefPubMed Szulewski A, Roth N, Howes D. The use of task-evoked pupillary response as an objective measure of cognitive load in novices and trained physicians: a new tool for the assessment of expertise. Acad Med. 2015;90:981–7.CrossRefPubMed
17.
go back to reference Alamudun F, Yoon H-J, Hammond T, Hudson K, Morin-Ducote G, Tourassi G. Shapelet analysis of pupil dilation for modeling visuo-cognitive behavior in screening mammography. In SPIE Medical Imaging. Edited by Abbey CK, Kupinski MA. San Diego, CA, USA: International Society for Optics and Photonics; 2016. 97870 M. Alamudun F, Yoon H-J, Hammond T, Hudson K, Morin-Ducote G, Tourassi G. Shapelet analysis of pupil dilation for modeling visuo-cognitive behavior in screening mammography. In SPIE Medical Imaging. Edited by Abbey CK, Kupinski MA. San Diego, CA, USA: International Society for Optics and Photonics; 2016. 97870 M.
18.
go back to reference Mello-Thoms C, Hardesty L, Sumkin J, Ganott M, Hakim C, Britton C, Stalder J, Maitz G. Effects of lesion conspicuity on visual search in mammogram reading. Acad Radiol. 2005;12:830–40. Mello-Thoms C, Hardesty L, Sumkin J, Ganott M, Hakim C, Britton C, Stalder J, Maitz G. Effects of lesion conspicuity on visual search in mammogram reading. Acad Radiol. 2005;12:830–40.
19.
go back to reference Elmore JG, Longton GM, Carney PA, Geller BM, Onega T, Tosteson ANA, Nelson HD, Pepe MS, Allison KH, Schnitt SJ, O’Malley FP, Weaver DL. Diagnostic concordance among pathologists interpreting breast biopsy specimens. JAMA. 2015;313:1122. Elmore JG, Longton GM, Carney PA, Geller BM, Onega T, Tosteson ANA, Nelson HD, Pepe MS, Allison KH, Schnitt SJ, O’Malley FP, Weaver DL. Diagnostic concordance among pathologists interpreting breast biopsy specimens. JAMA. 2015;313:1122.
20.
go back to reference Oster N, Carney PA, Allison KH, Weaver DL, Reisch LM, Longton G, Onega T, Pepe M, Geller BM, Nelson HD, Ross TR, Tosteson AN, Elmore JG. Development of a diagnostic test set to assess agreement in breast pathology: practical application of the guidelines for reporting reliability and agreement studies (GRRAS). BMS Womens Heal. 2013;13:3. Oster N, Carney PA, Allison KH, Weaver DL, Reisch LM, Longton G, Onega T, Pepe M, Geller BM, Nelson HD, Ross TR, Tosteson AN, Elmore JG. Development of a diagnostic test set to assess agreement in breast pathology: practical application of the guidelines for reporting reliability and agreement studies (GRRAS). BMS Womens Heal. 2013;13:3.
21.
go back to reference Allison KH, Reisch LM, Carney PA, Weaver DL, Schnitt SJ, O’Malley FP, Geller BM, Elmore JG. Understanding diagnostic variability in breast pathology: lessons learned from an expert consensus review panel. Histopathology. 2014;65:240–51. Allison KH, Reisch LM, Carney PA, Weaver DL, Schnitt SJ, O’Malley FP, Geller BM, Elmore JG. Understanding diagnostic variability in breast pathology: lessons learned from an expert consensus review panel. Histopathology. 2014;65:240–51.
23.
go back to reference Duchowski AT. Eye tracking methodology: theory and practice, vol. 55. New York: Springer; 2007. Duchowski AT. Eye tracking methodology: theory and practice, vol. 55. New York: Springer; 2007.
24.
go back to reference Henckens MJAG, Hermans EJ, Pu Z, Joëls M, Fernández G. Stressed memories: how acute stress affects memory formation in humans. J Neurosci. 2009;29:10111–9.CrossRefPubMed Henckens MJAG, Hermans EJ, Pu Z, Joëls M, Fernández G. Stressed memories: how acute stress affects memory formation in humans. J Neurosci. 2009;29:10111–9.CrossRefPubMed
25.
go back to reference Graber ML, Kissam S, Payne VL, Meyer AND, Sorensen A, Lenfestey N, Tant E, Henriksen K, Labresh K, Singh H. Cognitive interventions to reduce diagnostic error: a narrative review. BMJ Qual Saf. 2012;21:535–57. Graber ML, Kissam S, Payne VL, Meyer AND, Sorensen A, Lenfestey N, Tant E, Henriksen K, Labresh K, Singh H. Cognitive interventions to reduce diagnostic error: a narrative review. BMJ Qual Saf. 2012;21:535–57.
26.
go back to reference Graf S, Lin F, Kinshuk, McGreal R. Intelligent and Adaptive Learning Systems: Technology Enhanced Support for Learners and Teachers. Hershey, PA: IGI Global; 2012. Graf S, Lin F, Kinshuk, McGreal R. Intelligent and Adaptive Learning Systems: Technology Enhanced Support for Learners and Teachers. Hershey, PA: IGI Global; 2012.
27.
go back to reference Krupinski EA. Visual search of mammographic images: influence of lesion subtlety. Acad Radiol. 2005;12:965–9.CrossRefPubMed Krupinski EA. Visual search of mammographic images: influence of lesion subtlety. Acad Radiol. 2005;12:965–9.CrossRefPubMed
28.
go back to reference Kundel HL, Nodine CF, Krupinski EA, Mello-Thoms C. Using gaze-tracking data and mixture distribution analysis to support a holistic model for the detection of cancers on mammograms. Acad Radiol. 2008;15:881–6.CrossRefPubMed Kundel HL, Nodine CF, Krupinski EA, Mello-Thoms C. Using gaze-tracking data and mixture distribution analysis to support a holistic model for the detection of cancers on mammograms. Acad Radiol. 2008;15:881–6.CrossRefPubMed
29.
go back to reference Raghunath V, Braxton MO, Gagnon SA, Brunyé TT, Allison KH, Reisch LM, Weaver DL, Elmore JG, Shapiro LG. Mouse cursor movement and eye tracking data as an indicator of pathologists’ attention when viewing digital whole slide images. J Pathol Inform. 2012;3:43. Raghunath V, Braxton MO, Gagnon SA, Brunyé TT, Allison KH, Reisch LM, Weaver DL, Elmore JG, Shapiro LG. Mouse cursor movement and eye tracking data as an indicator of pathologists’ attention when viewing digital whole slide images. J Pathol Inform. 2012;3:43.
30.
go back to reference Klingner J, Rakshit Kumar PH. Measuring the task-evoked pupillary response with a remote eye tracker. In proceedings of the 2008 symposium on Eye tracking research & applications. Savannah: ACM; 2008. Klingner J, Rakshit Kumar PH. Measuring the task-evoked pupillary response with a remote eye tracker. In proceedings of the 2008 symposium on Eye tracking research & applications. Savannah: ACM; 2008.
31.
go back to reference Mercan E, Aksoy S, Shapiro LG, Weaver DL, Brunyé TT, Elmore JG: Localization of diagnostically relevant regions of interest in whole slide images: A comparative study. J Digit Imaging 2016, 10.1007/s10278-016-9873-1. Mercan E, Aksoy S, Shapiro LG, Weaver DL, Brunyé TT, Elmore JG: Localization of diagnostically relevant regions of interest in whole slide images: A comparative study. J Digit Imaging 2016, 10.​1007/​s10278-016-9873-1.
32.
go back to reference Ghaznavi F, Evans A, Madabhushi A, Feldman M. Digital imaging in pathology: whole-slide imaging and beyond. Annu Rev Pathol Mech Dis. 2013;8:331–59.CrossRef Ghaznavi F, Evans A, Madabhushi A, Feldman M. Digital imaging in pathology: whole-slide imaging and beyond. Annu Rev Pathol Mech Dis. 2013;8:331–59.CrossRef
Metadata
Title
Pupil diameter changes reflect difficulty and diagnostic accuracy during medical image interpretation
Authors
Tad T. Brunyé
Marianna D. Eddy
Ezgi Mercan
Kimberly H. Allison
Donald L. Weaver
Joann G. Elmore
Publication date
01-12-2016
Publisher
BioMed Central
Published in
BMC Medical Informatics and Decision Making / Issue 1/2016
Electronic ISSN: 1472-6947
DOI
https://doi.org/10.1186/s12911-016-0322-3

Other articles of this Issue 1/2016

BMC Medical Informatics and Decision Making 1/2016 Go to the issue