The vertical position of visual information conditions spatial memory performance in healthy aging.
Journal
Communications psychology
ISSN: 2731-9121
Titre abrégé: Commun Psychol
Pays: England
ID NLM: 9918716686206676
Informations de publication
Date de publication:
25 Jul 2023
25 Jul 2023
Historique:
received:
15
11
2022
accepted:
10
05
2023
medline:
25
7
2023
pubmed:
25
7
2023
entrez:
6
9
2024
Statut:
epublish
Résumé
Memory for objects and their location is a cornerstone of adequate cognitive functioning across the lifespan. Considering that human visual perception depends on the position of stimuli within the visual field, we posit that the position of objects in the environment may be a determinant aspect of mnemonic performance. In this study, a population of 25 young and 20 older adults completed a source-monitoring task with objects presented in the upper or lower visual field. Using standard Pr and multinomial processing tree analyses, we revealed that although familiarity-based item memory remained intact in older age, spatial memory was impaired for objects presented in the upper visual field. Spatial memory in aging is conditioned by the vertical position of information. These findings raise questions about the view that age-related spatial mnemonic deficits are attributable to associative dysfunctions and suggest that they could also originate from the altered encoding of object attributes.
Identifiants
pubmed: 39242667
doi: 10.1038/s44271-023-00002-3
pii: 10.1038/s44271-023-00002-3
doi:
Types de publication
Journal Article
Langues
eng
Pagination
2Subventions
Organisme : Agence Nationale de la Recherche (French National Research Agency)
ID : ANR-10-LABX-65
Organisme : Agence Nationale de la Recherche (French National Research Agency)
ID : ANR-18-IAHU-01
Informations de copyright
© 2023. The Author(s).
Références
Segen, V., Avraamides, M. N., Slattery, T. J. & Wiener, J. M. Age-related differences in visual encoding and response strategies contribute to spatial memory deficits. Mem. Cogn. 49, 249–264 (2021).
doi: 10.3758/s13421-020-01089-3
Klencklen, G., Després, O. & Dufour, A. What do we know about aging and spatial cognition? Reviews and perspectives. Ageing Res. Rev. 11, 123–135 (2012).
pubmed: 22085884
doi: 10.1016/j.arr.2011.10.001
Cheke, L. G. What-where-when memory and encoding strategies in healthy aging. Learn. Mem. 23, 121–126 (2016).
pubmed: 26884230
pmcid: 4755263
doi: 10.1101/lm.040840.115
Monge, Z. A. & Madden, D. J. Linking cognitive and visual perceptual decline in healthy aging: The information degradation hypothesis. Neurosci. Biobehav. Rev. 69, 166–173 (2016).
pubmed: 27484869
pmcid: 5030166
doi: 10.1016/j.neubiorev.2016.07.031
Nagarajan, N. et al. Vision impairment and cognitive decline among older adults: a systematic review. BMJ Open 12, e047929 (2022).
pubmed: 34992100
pmcid: 8739068
doi: 10.1136/bmjopen-2020-047929
Rezaul Karim, A. K. M. & Kojima, H. The what and why of perceptual asymmetries in the visual domain. Adv. Cogn. Psychol. 6, 103–115 (2010).
doi: 10.2478/v10053-008-0080-6
Abrams, J., Nizam, A. & Carrasco, M. Isoeccentric locations are not equivalent: the extent of the vertical meridian asymmetry. Vision Res. 52, 70–78 (2012).
pubmed: 22086075
doi: 10.1016/j.visres.2011.10.016
Corbett, J. E. & Carrasco, M. Visual performance fields: frames of reference. PLoS One 6, e24470 (2011).
pubmed: 21931727
pmcid: 3169603
doi: 10.1371/journal.pone.0024470
Carrasco, M., Talgar, C. P. & Cameron, E. L. Characterizing visual performance fields: effects of transient covert attention, spatial frequency, eccentricity, task and set size. Spat. Vis. 15, 61–75 (2002).
doi: 10.1163/15685680152692015
Hanning, N. M., Himmelberg, M. M. & Carrasco, M. Presaccadic attention enhances contrast sensitivity, but not at the upper vertical meridian. iScience 25, 103851 (2022).
pubmed: 35198902
pmcid: 8850791
doi: 10.1016/j.isci.2022.103851
Purokayastha, S., Roberts, M. & Carrasco, M. Voluntary attention improves performance similarly around the visual field. Atten. Percept. Psychophys. 83, 2784–2794 (2021).
pubmed: 34036535
pmcid: 8514247
doi: 10.3758/s13414-021-02316-y
Roberts, M., Cymerman, R., Theodore Smith, R., Kiorpes, L. & Carrasco, M. Covert spatial attention is functionally intact in amblyopic human adults. J. Vis. 16, 30 (2016).
pubmed: 28033433
pmcid: 5215291
doi: 10.1167/16.15.30
Skrandies, W. The upper and lower visual field of man: electrophysiological and functional differences. Prog. Sens. Phys. 8, 1–93 (1987).
doi: 10.1007/978-3-642-71060-5_1
Christman, S. D. & Niebauer, C. L. The relation between left-right and upper-lower visual field asymmetries. Adv. Psychol. 123, 263–296 (1997).
doi: 10.1016/S0166-4115(97)80076-3
Rezec, A. A. & Dobkins, K. R. Attentional weighting: a possible account of visual field asymmetries in visual search? Spat. Vis. 17, 269–293 (2004).
pubmed: 15559106
doi: 10.1163/1568568041920203
Levine, M. W. & McAnany, J. J. The relative capabilities of the upper and lower visual hemifields. Vision Res. 45, 2820–2830 (2005).
pubmed: 16051308
doi: 10.1016/j.visres.2005.04.001
Edwards, M. & Badcock, D. R. Motion distorts perceived depth. Vision Res. 43, 1799–1804 (2003).
pubmed: 12826103
doi: 10.1016/S0042-6989(03)00307-9
Lakha, L. & Humphreys, G. Lower visual field advantage for motion segmentation during high competition for selection. Spat. Vis. 18, 447–460 (2005).
pubmed: 16167776
doi: 10.1163/1568568054389570
Raymond, J. E. Directional anisotropy of motion sensitivity across the visual field. Vision Res. 34, 1029–1037 (1994).
pubmed: 8160412
doi: 10.1016/0042-6989(94)90007-8
Regan, D., Erkelens, C. J. & Collewijn, H. Visual field defects for vergence eye movements and for stereomotion perception. Investig. Ophthalmol. Vis. Sci. 27, 806–819 (1986).
Pflugshaupt, T. et al. Linking physiology with behaviour: functional specialisation of the visual field is reflected in gaze patterns during visual search. Vision Res. 49, 237–248 (2009).
pubmed: 19022277
doi: 10.1016/j.visres.2008.10.021
Previc, F. H. & Naegele, P. D. Target-tilt and vertical-hemifield asymmetries in free-scan search for 3-D targets. Percept. Psychophys. 63, 445–457 (2001).
pubmed: 11414132
doi: 10.3758/BF03194411
Rutkowski, J. S., Crewther, D. P. & Crewther, S. G. Normal readers have an upper visual field advantage in change detection. Clin. Experiment. Op. 30, 227–330 (2002).
doi: 10.1046/j.1442-9071.2002.00509.x
Carlei, C., Framorando, D., Burra, N. & Kerzel, D. Face processing is enhanced in the left and upper visual hemi-fields. Vis. cogn. 25, 749–761 (2017).
doi: 10.1080/13506285.2017.1327466
Feng, J. & Spence, I. Upper visual field advantage in localizing a target among distractors. Iperception. 5, 97–100 (2014).
pubmed: 25469215
pmcid: 4249996
Goldstein, A. & Babkoff, H. A comparison of upper vs. lower and right vs. left visual fields using lexical decision. Q. J. Exp. Psychol. A 54, 1239–1259 (2001).
pubmed: 11765742
doi: 10.1080/713756008
Niebauer, C. L. & Christman, S. D. Upper and lower visual field differences in categorical and coordinate judgments. Psychon. Bull. Rev. 5, 147–151 (1998).
doi: 10.3758/BF03209471
Genzano, V. R., Di Nocera, F. & Ferlazzo, F. Upper/lower visual field asymmetry on a spatial relocation memory task. Neuroreport 12, 1227–1230 (2001).
pubmed: 11338196
doi: 10.1097/00001756-200105080-00034
Montaser-Kouhsari, L. & Carrasco, M. Perceptual asymmetries are preserved in short-term memory tasks. Atten. Percept. Psychophys. 71, 1782–1792 (2009).
pubmed: 19933562
pmcid: 3697833
doi: 10.3758/APP.71.8.1782
Carrasco, M., Roberts, M., Myers, C. & Shukla, L. Visual field asymmetries vary between children and adults. Curr. Biol. 32, R509–R510 (2022).
pubmed: 35671720
pmcid: 9278050
doi: 10.1016/j.cub.2022.04.052
Tsurumi, S., Kanazawa, S., Yamaguchi, M. K. & Kawahara, J. I. Development of upper visual field bias for faces in infants. Dev. Sci. 26, e13262 (2022).
pubmed: 35340093
pmcid: 10078383
Cherry, K. E. & Park, D. C. Age-related differences in three-dimensional spatial memory. J. Gerontol. 44, 16–22 (1989).
doi: 10.1093/geronj/44.1.P16
Erel, H., Ronen, T., Freedman, G., Deouell, L. Y. & Levy, D. A. Preserved left and upper visual field advantages in older adults’ orienting of attention. Exp. Gerontol. 124, 110630 (2019).
pubmed: 31195104
doi: 10.1016/j.exger.2019.110630
Feng, J. et al. Differential age-related changes in localizing a target among distractors across an extended visual field. Eur. J. Ageing 14, 167–177 (2017).
pubmed: 28804400
doi: 10.1007/s10433-016-0399-7
Brennan, A. A., Bruderer, A. J., Liu-Ambrose, T., Handy, T. C. & Enns, J. T. Lifespan changes in attention revisited: everyday visual search. Can. J. Exp. Psychol. 71, 160–171 (2017).
pubmed: 28604052
doi: 10.1037/cep0000130
Silva, M. F., D’Almeida, O. C., Oliveiros, B., Mateus, C. & Castelo-Branco, M. Development and aging of visual hemifield asymmetries in contrast sensitivity. J. Vis. 14, 19 (2014).
pubmed: 25326605
doi: 10.1167/14.12.19
Lagrené, K. et al. Healthy and pathological visual aging in a French follow-up cohort study. Invest. Ophthalmol. Vis. Sci. 60, 5915 (2019).
Folstein, M. F., Folstein, S. E. & McHugh, P. R. ‘Mini-mental state’. A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 12, 189–198 (1975).
pubmed: 1202204
doi: 10.1016/0022-3956(75)90026-6
Kozhevnikov, M. & Hegarty, M. A dissociation between object manipulation spatial ability and spatial orientation ability. Mem. Cogn. 29, 745–756 (2001).
doi: 10.3758/BF03200477
Corsi, P. M. Human memory and the medial temporal region of the brain. Dissertatopm Abstr. Int. 34, 891 (1973).
Vandenberg, S. G. & Kuse, A. R. Mental rotations, a group test of three-dimensional spatial visualization. Percept. Mot. Skills 47, 599–604 (1978).
pubmed: 724398
doi: 10.2466/pms.1978.47.2.599
Peirce, J. et al. PsychoPy2: Experiments in behavior made easy. Behav. Res. Methods 51, 195–203 (2019).
pubmed: 30734206
pmcid: 6420413
doi: 10.3758/s13428-018-01193-y
Stark, S. M., Kirwan, C. B. & Stark, C. E. L. Mnemonic similarity task: a tool for assessing hippocampal integrity. Trends Cogn. Sci. 23, 938–951 (2019).
pubmed: 31597601
pmcid: 6991464
doi: 10.1016/j.tics.2019.08.003
Brady, T. F., Konkle, T., Alvarez, G. A. & Oliva, A. Visual long-term memory has a massive storage capacity for object details. Proc. Natl. Acad. Sci. USA. 105, 14325–14329 (2008).
pubmed: 18787113
pmcid: 2533687
doi: 10.1073/pnas.0803390105
Yonelinas, A. P. The contribution of recollection and familiarity to recognition and source-memory judgments: a formal dual-process model and an analysis of receiver operating characteristics. J. Exp. Psychol. Learn. Mem. Cogn. 25, 1415–1434 (1999).
pubmed: 10605829
doi: 10.1037/0278-7393.25.6.1415
von der Malsburg, T. Saccades: detection of fixations in eyetracking data. Retrieved from https://github.com/tmalsburg/saccades (2019).
Fujii, G. Y. et al. Patient selection for macular translocation surgery using the scanning laser ophthalmoscope. Ophthalmology 109, 1737–1744 (2002).
pubmed: 12208725
doi: 10.1016/S0161-6420(02)01120-X
Schönbach, E. M. et al. Metrics and acquisition modes for fixation stability as a visual function biomarker. Investig. Ophthalmol. Vis. Sci. 58, BIO268–BIO276 (2017).
doi: 10.1167/iovs.17-21710
Snodgrass, J. G. & Corwin, J. Pragmatics of measuring recognition memory: applications to dementia and amnesia. J. Exp. Psychol. Gen. 117, 34–50 (1988).
pubmed: 2966230
doi: 10.1037/0096-3445.117.1.34
Bates, D. M., Kliegl, R., Vasishth, S. & Baayen, H. Parsimonious mixed models. Preprint at https://doi.org/10.48550/arXiv.1506.04967 (2015).
Lo, S. & Andrews, S. To transform or not to transform: using generalized linear mixed models to analyse reaction time data. Front. Psychol. 6, 1171 (2015).
pubmed: 26300841
pmcid: 4528092
doi: 10.3389/fpsyg.2015.01171
Riefer, D. M. & Batchelder, W. H. Multinomial modeling and the measurement of cognitive processes. Psychol. Rev. 95, 318–339 (1988).
doi: 10.1037/0033-295X.95.3.318
Erdfelder, E. et al. Multinomial processing tree models: a review of the literature. J. Psychol. 217, 108–124 (2009).
Batchelder, W. H. & Riefer, D. M. Multinomial processing models of source monitoring. Psychol. Rev. 97, 548–564 (1990).
doi: 10.1037/0033-295X.97.4.548
Bröder, A. & Meiser, T. Measuring source memory. J. Psychol. 215, 52–60 (2007).
Cooper, E., Greve, A. & Henson, R. N. Assumptions behind scoring source versus item memory: effects of age, hippocampal lesions and mild memory problems. Cortex 91, 297–315 (2017).
pubmed: 28162777
pmcid: 5460522
doi: 10.1016/j.cortex.2017.01.001
Yonelinas, A. P., Aly, M., Wang, W. C. & Koen, J. D. Recollection and familiarity: examining controversial assumptions and new directions. Hippocampus 20, 1178–1194 (2010).
pubmed: 20848606
pmcid: 4251874
doi: 10.1002/hipo.20864
Heck, D. W., Arnold, N. R. & Arnold, D. TreeBUGS: an R package for hierarchical multinomial-processing-tree modeling. Behav. Res. Methods 50, 264–284 (2018).
pubmed: 28374146
doi: 10.3758/s13428-017-0869-7
Klauer, K. C. Hierarchical multinomial processing tree models: a latent-trait approach. Psychometrika 75, 70–98 (2010).
doi: 10.1007/s11336-009-9141-0
Himmelberg, M. M., Winawer, J. & Carrasco, M. Linking individual differences in human primary visual cortex to contrast sensitivity around the visual field. Nat. Commun. 13, 1–13 (2022).
doi: 10.1038/s41467-022-31041-9
Bastin, C. & Van Der Linden, M. The effects of aging on the recognition of different types of associations. Exp. Aging Res. 32, 61–77 (2005).
doi: 10.1080/03610730500326291
Chalfonte, B. L. & Johnson, M. K. Feature memory and binding in young and older adults. Mem. Cogn. 24, 403–416 (1996).
doi: 10.3758/BF03200930
Naveh-Benjamin, M. Adult age differences in memory performance: tests of an associative deficit hypothesis. J. Exp. Psychol. Learn. Mem. Cogn. 26, 1170–1187 (2000).
pubmed: 11009251
doi: 10.1037/0278-7393.26.5.1170
Toner, C. K., Pirogovsky, E., Kirwan, C. B. & Gilbert, P. E. Visual object pattern separation deficits in nondemented older adults. Learn. Mem. 16, 338–342 (2009).
pubmed: 19403797
doi: 10.1101/lm.1315109
Schiavetto, A., Köhler, S., Grady, C. L., Winocur, G. & Moscovitch, M. Neural correlates of memory for object identity and object location: effects of aging. Neuropsychologia 40, 1428–1442 (2002).
pubmed: 11931947
doi: 10.1016/S0028-3932(01)00206-8
Bender, A. R., Naveh-Benjamin, M. & Raz, N. Associative deficit in recognition memory in a lifespan sample of healthy adults. Psychol. Aging 25, 940–948 (2010).
pubmed: 20822256
pmcid: 3011045
doi: 10.1037/a0020595
Naveh-Benjamin, M., Hussain, Z., Guez, J. & Bar-On, M. Adult age differences in episodic memory: further support for an associative-deficit hypothesis. J. Exp. Psychol. Learn. Mem. Cogn. 29, 826–837 (2003).
pubmed: 14516216
doi: 10.1037/0278-7393.29.5.826
Old, S. R. & Naveh-Benjamin, M. Differential effects of age on item and associative measures of memory: a meta-analysis. Psychol. Aging 23, 104–118 (2008).
pubmed: 18361660
doi: 10.1037/0882-7974.23.1.104
Koen, J. D. & Yonelinas, A. P. Recollection, not familiarity, decreases in healthy ageing: converging evidence from four estimation methods. Memory 24, 75–88 (2016).
pubmed: 25485974
doi: 10.1080/09658211.2014.985590
McIntyre, J. S. & Craik, F. I. Age differences in memory for item and source information. Can. J. Psychol. 41, 175–192 (1987).
pubmed: 3502895
doi: 10.1037/h0084154
Hagenbeek, R. E. & Van Strien, J. W. Left-right and upper-lower visual field asymmetries for face matching, letter naming, and lexical decision. Brain Cogn. 49, 34–44 (2002).
pubmed: 12027390
doi: 10.1006/brcg.2001.1481
Quek, G. L. & Finkbeiner, M. Face-sex categorization is better above fixation than below: evidence from the reach-to-touch paradigm. Cogn. Affect. Behav. Neurosci. 14, 1407–1419 (2014).
pubmed: 24763922
doi: 10.3758/s13415-014-0282-y
Quek, G. L. & Finkbeiner, M. Gaining the upper hand: evidence of vertical asymmetry in sex-categorisation of human hands. Adv. Cogn. Psychol. 10, 131–143 (2014).
pubmed: 25674193
pmcid: 4313869
doi: 10.5709/acp-0164-8
Quek, G. L. & Finkbeiner, M. The upper-hemifield advantage for masked face processing: not just an attentional bias. Atten. Percept. Psychophys. 78, 52–68 (2016).
pubmed: 26515816
doi: 10.3758/s13414-015-0965-7
Kupers, E. R., Carrasco, M. & Winawer, J. Modeling visual performance differences ‘around’ the visual field: a computational observer approach. PLoS Comput. Biol. 15, e1007063 (2019).
pubmed: 31125331
pmcid: 6553792
doi: 10.1371/journal.pcbi.1007063
Barbot, A., Xue, S. & Carrasco, M. Asymmetries in visual acuity around the visual field. J. Vis. 21, 2 (2021).
pubmed: 33393963
pmcid: 7794272
doi: 10.1167/jov.21.1.2
Danckert, J. & Goodale, M. A. Superior performance for visually guided pointing in the lower visual field. Exp. Brain Res. 137, 303–308 (2001).
pubmed: 11355377
doi: 10.1007/s002210000653
Previc, F. H. Functional specialization in the lower and upper visual fields in humans: Its ecological origins and neurophysiological implications. Behav. Brain Sci. 13, 519–542 (1990).
doi: 10.1017/S0140525X00080018
Sayres, R. & Grill-Spector, K. Relating retinotopic and object-selective responses in human lateral occipital cortex. J. Neurophysiol. 100, 249–267 (2008).
pubmed: 18463186
pmcid: 2493478
doi: 10.1152/jn.01383.2007
Strother, L., Aldcroft, A., Lavell, C. & Vilis, T. Equal degrees of object selectivity for upper and lower visual field stimuli. J. Neurophysiol. 104, 2075–2081 (2010).
pubmed: 20719923
doi: 10.1152/jn.00462.2010
Niemeier, M., Goltz, H. C., Kuchinad, A., Tweed, D. B. & Vilis, T. A contralateral preference in the lateral occipital area: sensory and attentional mechanisms. Cereb. Cortex 15, 325–331 (2005).
pubmed: 15269109
doi: 10.1093/cercor/bhh134
Yassa, M. A. & Stark, C. E. L. Pattern separation in the hippocampus. Trends Neurosci. 34, 515–525 (2011).
pubmed: 21788086
pmcid: 3183227
doi: 10.1016/j.tins.2011.06.006
Durteste, M. et al. The vertical position of visual information conditions spatial memory performance in healthy aging. OSF. https://doi.org/10.17605/OSF.IO/UNBY4 (2023).