Gaze Fixation Patterns Correlate with Visual Attention and Memory: the Results of a Pilot Study in Healthy Subjects

Danilov G.V., Vigasina K.S., Strunina Yu.V., Kaverina M.A., Galkin M.V., Kuleva A.Yu., Alekseeva A.N., Lazutkin A.A., Enikolopov G.N., Krotkova O.A.

Key words: eye tracking; spatial distribution of attention; memory; recognition errors of visual stimuli; pattern separation; hippocampus.

2019, volume 11, issue 1, page 54.

DOI: https://doi.org/10.17691/stm2019.11.1.06

Full text

html pdf

2176

1614

Abstract
References
How to cite

In recent years, distinguishing between similar short-term memory traces (pattern separation) in humans and animals has become an important part of neurophysiological research aimed to localize these functions in the brain.

The aim of this study was to assess the spatial gaze distribution in healthy subjects with a specific pattern separation error detected in visual attention and memory tests using the eye tracking technology.

Materials and Methods. The 45 healthy volunteers were enrolled in the study and divided into two independent groups. In group 1 (28 subjects aged from 19 to 78 years old), the age-related features of visual fixations distribution were studied in the task of distinguishing similar objects. In group 2 (17 subjects aged 19 to 25), the distribution of visual attention in specific areas of the object was investigated. An original neuropsychological method was used: visual stimuli, eye tracking and subsequent assessment of stimuli recall and recognition.

Results. We found significant differences in the distribution of visual fixations between the younger and older groups (p<0.05), as well as in the occurrence of pattern separation errors (p<0.05). The obtained data support the hypothesis of different physiological mechanisms that control the spatial distribution of visual attention in subjects of different ages.

Stern C.E., Corkin S., González R.G., Guimaraes A.R., Baker J.R., Jennings P.J., Carr C.A., Sugiura R.M., Vedantham V., Rosen B.R. The hippocampal formation participates in novel picture encoding: evidence from functional magnetic resonance imaging. Proc Natl Acad Sci U S A 1996; 93(16): 8660–8665, https://doi.org/10.1073/pnas.93.16.8660.
Yassa M.A., Stark C.E.L. Pattern separation in the hippocampus. Trends Neurosci 2011; 34(10): 515–525, https://doi.org/10.1016/j.tins.2011.06.006.
Stark S.M., Yassa M.A., Lacy J.W., Stark C.E.L. A task to assess behavioral pattern separation (BPS) in humans: data from healthy aging and mild cognitive impairment. Neuropsychologia 2013; 51(12): 2442–2449, https://doi.org/10.1016/j.neuropsychologia.2012.12.014.
Dillon S.E., Tsivos D., Knight M., McCann B., Pennington C., Shiel A.I., Conway M.E., Newson M.A., Kauppinen R.A., Coulthard E.J. The impact of ageing reveals distinct roles for human dentate gyrus and CA3 in pattern separation and object recognition memory. Sci Rep 2017; 7(1): 14069, https://doi.org/10.1038/s41598-017-13853-8.
Bakker A., Kirwan C.B., Miller M., Stark C.E.L. Pattern separation in the human hippocampal CA3 and dentate gyrus. Science 2008; 319(5870): 1640–1642, https://doi.org/10.1126/science.1152882.
Molitor R.J., Ko P.C., Hussey E.P., Ally B.A. Memory-related eye movements challenge behavioral measures of pattern completion and pattern separation. Hippocampus 2014; 24(6): 666–672, https://doi.org/10.1002/hipo.22256.
Kassab R., Alexandre F. Pattern separation in the hippocampus: distinct circuits under different conditions. Brain Struct Funct 2018; 223(6): 2785–2808, https://doi.org/10.1007/s00429-018-1659-4.
Loftus G.R. Eye fixations and recognition memory for pictures. Cogn Psychol 1972; 3(4): 525–551, https://doi.org/10.1016/0010-0285(72)90021-7.
Shelton J.T., Christopher E.A. A fresh pair of eyes on prospective memory monitoring. Mem Cognit 2016; 44(6): 837–845, https://doi.org/10.3758/s13421-016-0601-3.
Steinmetz K.R.M., Kensinger E.A. The emotion-induced memory trade-off: more than an effect of overt attention? Mem Cognit 2013; 41(1): 69–81, https://doi.org/10.3758/s13421-012-0247-8.
Hannula D.E. Worth a glance: using eye movements to investigate the cognitive neuroscience of memory. Front Hum Neurosci 2010; 4: 166, https://doi.org/10.3389/fnhum.2010.00166.
Korsakova N.K., Roshchina I.F. Znachenie kontseptsii A.R. Lurii o trekh funktsional’nykh blokakh mozga dlya stanovleniya i razvitiya neyrogerontopsikhologii. V kn.: Nasledie A.R. Lurii v sovremennom nauchnom i kul’turno-istoricheskom kontekste [The value of A.R. Luria’s concept about functional brain blocks for formation and development of neurogerontopsychology. In: A.R. Luria’s heritage in modern scientific and cultural-historic context]. Moscow; 2012; p. 161–176.
Krotkova O.A., Kaverina M.Y., Danilov G.V. Eye tracking and interhemispheric interaction in the distribution of spatial attention. Hum Physiol 2018; 44(2): 175–182, https://doi.org/10.1134/s0362119718020123.
Voss J.L., Bridge D.J., Cohen N.J., Walker J.A. A closer look at the hippocampus and memory. Trends Cogn Sci 2017; 21(8): 577–588, https://doi.org/10.1016/j.tics.2017.05.008.
Cohen K.B., Glass B., Greiner H.M., Holland-Bouley K., Standridge S., Arya R., Faist R., Morita D., Mangano F., Connolly B., Glauser T., Pestian J. Methodological issues in predicting pediatric epilepsy surgery candidates through natural language processing and machine learning. Biomed Inform Insights 2016; 8: BII.S38308, https://doi.org/10.4137/bii.s38308.
Danilov G.V., Krotkova O.A., Kaverina M.Yu., Sharova E.V., Yarets M.Yu., Kuleva A.Yu., Smirnov A.S., Zakharov V.O., Vigasina K.D., Strunina Yu.V. Primenenie tekhnologii aytrekinga dlya psikhofiziologicheskikh issledovaniy v neyrokhirurgii i reabilitatsii bol’nykh s vyrazhennymi narusheniyami dvigatel’nykh i kommunikativnykh funktsiy. V kn.: III Mezhdunarodnaya nauchno-prakticheskaya konferentsiya po neyroreabilitatsii v neyrokhirurgii [Using the eye-tracking technology for psychophysiological investigations in neurosurgery and rehabilitation of patients with marked disorders of motor and communicative functions. In: III International scientific-practical conference on neurorehabilitation in neurosurgery]. Kazan; 2017; p. 65–68.
Krotkova О.А., Danilov G.V., Kaverina M.Y., Kuleva A.Y., Gavrilova E.V., Enikolopova E.V. The distribution of visual attention in normal aging: the eye tracking study. Moscow University Psychology Bulletin 2018; 1: 21–36, https://doi.org/10.11621/vsp.2018.01.21.
Henderson J.M., Williams C.C., Falk R.J. Eye movements are functional during face learning. Mem Cognit 2005; 33(1): 98–106, https://doi.org/10.3758/bf03195300.
Chan J.P.K., Kamino D., Binns M.A., Ryan J.D. Can changes in eye movement scanning alter the age-related deficit in recognition memory? Front Psychol 2011; 2: 92, https://doi.org/10.3389/fpsyg.2011.00092.
Lohnas L.J., Duncan K., Doyle W.K., Thesen T., Devinsky O., Davachi L. Time-resolved neural reinstatement and pattern separation during memory decisions in human hippocampus. Proc Natl Acad Sci U S A 2018; 115(31): E7418–E7427, https://doi.org/10.1073/pnas.1717088115.
Danilov G.V., Galkin M.V., Alekseeva A.N., Enikolopova E.V., Krotkova O.A. The impact of radiotherapy on visual attention and memory in patients with cavernous sinus meningioma: a pilot study. In: EANS 2017 Annual Meeting Controversies and Solutions in Neurosurgery. Venice, Italy; 2017.

Danilov G.V., Vigasina K.S., Strunina Yu.V., Kaverina M.A., Galkin M.V., Kuleva A.Yu., Alekseeva A.N., Lazutkin A.A., Enikolopov G.N., Krotkova O.A. Gaze Fixation Patterns Correlate with Visual Attention and Memory: the Results of a Pilot Study in Healthy Subjects. Sovremennye tehnologii v medicine 2019; 11(1): 54, https://doi.org/10.17691/stm2019.11.1.06