Abstract
Several times per second, humans make rapid eye movements called saccades which redirect their gaze to sample new regions of external space. Saccades present unique challenges to both perceptual and motor systems. During the movement, the visual input is smeared across the retina and severely degraded. Once completed, the projection of the world onto the retina has undergone a large-scale spatial transformation. The vector of this transformation, and the new orientation of the eye in the external world, is uncertain. Memory for the pre-saccadic visual input is thought to play a central role in compensating for the disruption caused by saccades. Here, we review evidence that memory contributes to (1) detecting and identifying changes in the world that occur during a saccade, (2) bridging the gap in input so that visual processing does not have to start anew, and (3) correcting saccade errors and recalibrating the oculomotor system to ensure accuracy of future saccades. We argue that visual working memory (VWM) is the most likely candidate system to underlie these behaviours and assess the consequences of VWM’s strict resource limitations for transsaccadic processing. We conclude that a full understanding of these processes will require progress on broader unsolved problems in psychology and neuroscience, in particular how the brain solves the object correspondence problem, to what extent prior beliefs influence visual perception, and how disparate signals arriving with different delays are integrated.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Albano JE, King WM (1989) Rapid adaptation of saccadic amplitude in humans and monkeys. Invest Ophthalmol Vis Sci 30:1883–1893
Atsma J, Maij F, Koppen M et al (2016) Causal inference for spatial constancy across saccades. PLoS Comput Biol 12:e1004766
Baddeley AD, Hitch G (1974) Working memory. Psychol Learn Motiv 8:47–89
Bahcall DO, Kowler E (2000) The control of saccadic adaptation: implications for the scanning of natural visual scenes. Vis Res 40:2779–2796
Barnes GR, Gresty MA (1973) Characteristics of eye movements to targets of short duration. Aerosp Med 44:1236–1240
Bays PM, Husain M (2008) Dynamic shifts of limited working memory resources in human vision. Science 321:851–854
Bays PM, Catalao RFG, Husain M (2009) The precision of visual working memory is set by allocation of a shared resource. J Vis 9(7):1–711
Bays PM, Wu EY, Husain M (2011) Storage and binding of object features in visual working memory. Neuropsychologia 49:1622–1631
Becker W (1976) Do correction saccades depend exclusively on retinal feedback? A note on the possible role of non-retinal feedback. Vis Res 16:425–427
Becker W, Fuchs AF (1969) Further properties of the human saccadic system: eye movements and correction saccades with and without visual fixation points. Vis Res 9:1247–1258
Boehnke SE, Munoz DP (2008) On the importance of the transient visual response in the superior colliculus. Curr Opin Neurobiol 18:544–551
Bonnetblanc F, Baraduc P (2007) Saccadic adaptation without retinal postsaccadic error. Neuroreport 18:1399–1402
Bremmer F, Kubischik M, Hoffmann K-P, Krekelberg B (2009) Neural dynamics of saccadic suppression. J Neurosci 29:12374–12383
Bridgeman B (2007) Efference copy and its limitations. Comput Biol Med 37:924–929
Bridgeman B, Mayer M (1983) Failure to integrate visual information from successive fixations. Bull Psychon Soc 21:285–286
Bridgeman B, Hendry D, Stark L (1975) Failure to detect displacement of the visual world during saccadic eye movements. Vis Res 15:719–722
Bridgeman B, Van Der Heijden CAH, Velichkovsky BM (1994) A theory of visual stability across saccadic eye movements. Behav Brain Sci 17:247–292
Burr DC, Morrone MC (2011) Spatiotopic coding and remapping in humans. Philos Trans R Soc Lond Ser B Biol Sci 366:504–515
Burr DC, Morrone MC, Ross J (1994) Selective suppression of the magnocellular visual pathway during saccadic eye movements. Nature 371:511–513
Castet E, Jeanjean S, Masson GS (2002) Motion perception of saccade-induced retinal translation. Proc Natl Acad Sci 99:15159–15163
Cavanagh P, Hunt AR, Afraz A, Rolfs M (2010) Visual stability based on remapping of attention pointers. Trends Cogn Sci 14:147–153
Collins T, Wallman J (2012) The relative importance of retinal error and prediction in saccadic adaptation. J Neurophysiol 107:3342–3348
Cowan N (2001) The magical number 4 in short-term memory: a reconsideration of mental storage capacity. Behav Brain Sci 24:87–114 Discussion 114–185
Cox DD, Meier P, Oertelt N, DiCarlo JJ (2005) “Breaking” position-invariant object recognition. Nat Neurosci 8:1145–1147
Currie CB, McConkie GW, Carlson-Radvansky LA, Irwin DE (2000) The role of the saccade target object in the perception of a visually stable world. Percept Psychophys 62:673–683
Demeyer M, de Graef P, Wagemans J, Verfaillie K (2010a) Parametric integration of visual form across saccades. Vis Res 50:1225–1234
Demeyer M, Graef PD, Wagemans J, Verfaillie K (2010b) Object form discontinuity facilitates displacement discrimination across saccades. J Vis 10:17–17
Deubel H (1991) Adaptive control of saccade metrics. In: Presbyopia research. Springer, Boston, pp 93–100
Deubel H (1995) Is saccadic adaptation context-specific? In: Findlay JM, Walker R, Kentridge RW (eds) Studies in visual information processing. North-Holland, Amsterdam, pp 177–187
Deubel H (2004) Localization of targets across saccades: role of landmark objects. Vis Cogn 11:173–202
Deubel H, Schneider WX (1996) Saccade target selection and object recognition: evidence for a common attentional mechanism. Vis Res 36:1827–1837
Deubel H, Wolf W, Hauske G (1982) Corrective saccades: effect of shifting the saccade goal. Vis Res 22:353–364
Deubel H, Schneider WX, Bridgeman B (1996) Postsaccadic target blanking prevents saccadic suppression of image displacement. Vis Res 36:985–996
Deubel H, Bridgeman B, Schneider WX (1998) Immediate post-saccadic information mediates space constancy. Vis Res 38:3147–3159
Deubel H, Schneider WX, Bridgeman B (2002) Transsaccadic memory of position and form. Prog Brain Res 140:165–180
Diamond MR, Ross J, Morrone MC (2000) Extraretinal control of saccadic suppression. J Neurosci 20:3449–3455
Ditterich J, Eggert T, Straube A (2000) The role of the attention focus in the visual information processing underlying saccadic adaptation. Vis Res 40:1125–1134
Dowiasch S, Marx S, Einhäuser W, Bremmer F (2015) Effects of aging on eye movements in the real world. Front Hum Neurosci 9:46
Fracasso A, Caramazza A, Melcher D (2010) Continuous perception of motion and shape across saccadic eye movements. J Vis 10:14
Ganmor E, Landy MS, Simoncelli EP (2015) Near-optimal integration of orientation information across saccades. J Vis 15:8
Gegenfurtner KR, Sperling G (1993) Information transfer in iconic memory experiments. J Exp Psychol Hum Percept Perform 19:845–866
Germeys F, de Graef P, Verfaillie K (2002) Transsaccadic perception of saccade target and flanker objects. J Exp Psychol Hum Percept Perform 28:868–883
Germeys F, Graef PD, Eccelpoel CV, Verfaillie K (2010) The visual analog: evidence for a preattentive representation across saccades. J Vis 10:9
Gigerenzer G, Brighton H (2009) Homo heuristicus: why biased minds make better inferences. Top Cogn Sci 1:107–143
Gordon RD, Irwin DE (1998) Eye movements, attention and trans-saccadic memory. Vis Cogn 5:127–155
Gorgoraptis N, Catalao RFG, Bays PM, Husain M (2011) Dynamic updating of working memory resources for visual objects. J Neurosci 31:8502–8511
Gysen V, de Graef P, Verfaillie K (2002a) Detection of intrasaccadic displacements and depth rotations of moving objects. Vis Res 42:379–391
Gysen V, Verfaillie K, de Graef P (2002b) Transsaccadic perception of translating objects: effects of landmark objects and visual field position. Vis Res 42:1785–1796
Hanning NM, Jonikaitis D, Deubel H, Szinte M (2015) Oculomotor selection underlies feature retention in visual working memory. J Neurophysiol 115:1071–1076
Harrison WJ, Bex PJ (2014) Integrating retinotopic features in spatiotopic coordinates. J Neurosci 34:7351–7360
Hayhoe M, Lachter J, Feldman J (1991) Integration of form across saccadic eye movements. Perception 20:393–402
Henderson JM (1992) Identifying objects across saccades: effects of extrafoveal preview and flanker object context. J Exp Psychol Learn Mem Cogn 18:521–530
Henderson JM (1994) Two representational systems in dynamic visual identification. J Exp Psychol Gen 123:410–426
Henderson JM, Anes MD (1994) Roles of object-file review and type priming in visual identification within and across eye fixations. J Exp Psychol Hum Percept Perform 20:826–839
Henderson JM, Hollingworth A (1999) The role of fixation position in detecting scene changes across saccades. Psychol Sci 10:438–443
Henderson JM, Hollingworth A (2003) Eye movements and visual memory: detecting changes to saccade targets in scenes. Percept Psychophys 65:58–71
Henderson JM, Siefert ABC (1999) The influence of enantiomorphic transformation on transsaccadic object integration. J Exp Psychol Hum Percept Perform 25:243–255
Henderson JM, Siefert ABC (2001) Types and tokens in transsaccadic object identification: effects of spatial position and left-right orientation. Psychon Bull Rev 8:753–760
Henderson JM, Pollatsek A, Rayner K (1987) Effects of foveal priming and extrafoveal preview on object identification. J Exp Psychol Hum Percept Perform 13:449–463
Herman JP, Blangero A, Madelain L et al (2013) Saccade adaptation as a model of flexible and general motor learning. Exp Eye Res 114:6–15
Higgins E, Rayner K (2015) Transsaccadic processing: stability, integration, and the potential role of remapping. Atten Percept Psychophys 77:3–27
Hollingworth A, Luck SJ (2009) The role of visual working memory in the control of gaze during visual search. Atten Percept Psychophys 71:936–949
Hollingworth A, Richard AM, Luck SJ (2008) Understanding the function of visual short-term memory: transsaccadic memory, object correspondence, and gaze correction. J Exp Psychol Gen 137:163–181
Hollingworth A, Matsukura M, Luck SJ (2013) Visual working memory modulates low-level saccade target selection: evidence from rapidly generated saccades in the global effect paradigm. J Vis 13:4
Hopp JJ, Fuchs AF (2004) The characteristics and neuronal substrate of saccadic eye movement plasticity. Prog Neurobiol 72:27–53
Hübner C, Schütz AC (2017) Numerosity estimation benefits from transsaccadic information integration. J Vis 17:12
Irwin DE (1992) Memory for position and identity across eye movements. J Exp Psychol Learn Mem Cogn 18:307–317
Irwin DE (1996) Integrating information across saccadic eye movements. Curr Dir Psychol Sci 5:94–100
Irwin DE, Andrews RV (1996) Integration and accumulation of information across saccadic eye movements. Atten Perform 16:122–155
Irwin DE, Zelinsky GJ (2002) Eye movements and scene perception: memory for things observed. Percept Psychophys 64:882–895
Irwin DE, Yantis S, Jonides J (1983) Evidence against visual integration across saccadic eye movements. Percept Psychophys 34:49–57
Irwin DE, Zacks JL, Brown JS (1990) Visual memory and the perception of a stable visual environment. Percept Psychophys 47:35–46
Jeyachandra J, Nam Y, Kim Y et al (2018) Transsaccadic memory of multiple spatially variant and invariant object features. J Vis 18:6
Jonides J, Irwin DE, Yantis S (1982) Integrating visual information from successive fixations. Science 215:192–194
Jonides J, Irwin DE, Yantis S (1983) Failure to integrate information from successive fixations. Science 222:188
Kahneman D, Treisman A, Gibbs BJ (1992) The reviewing of object files: object-specific integration of information. Cogn Psychol 24:175–219
Kersten D, Mamassian P, Yuille A (2004) Object perception as Bayesian inference. Annu Rev. Psychol 55:271–304
Knill DC, Pouget A (2004) The Bayesian brain: the role of uncertainty in neural coding and computation. Trends Neurosci 27:712–719
Li N, DiCarlo JJ (2008) Unsupervised natural experience rapidly alters invariant object representation in visual cortex. Science 321:1502–1507
Li W, Matin L (1990) The influence of saccade length on the saccadic suppression of displacement detection. Percept Psychophys 48:453–458
Luck SJ, Vogel EK (1997) The capacity of visual working memory for features and conjunctions. Nature 390:279–281
Ma WJ, Husain M, Bays PM (2014) Changing concepts of working memory. Nat Neurosci 17:347–356
Mackay DM (1972) Visual stability. Invest Ophthalmol Vis Sci 11:518–524
Madelain L, Harwood MR, Herman JP, Wallman J (2010) Saccade adaptation is unhampered by distractors. J Vis 10:29–29
Madelain L, Herman JP, Harwood MR (2013) Saccade adaptation goes for the goal. J Vis 13:9
McConkie GW, Currie CB (1996) Visual stability across saccades while viewing complex pictures. J Exp Psychol Hum Percept Perform 22:563–581
McConkie GW, Rayner K (1976) Asymmetry of the perceptual span in reading. Bull Psychon Soc 8:365–368
Melcher D, Colby CL (2008) Trans-saccadic perception. Trends Cogn Sci 12:466–473
Melcher D, Kowler E (2001) Visual scene memory and the guidance of saccadic eye movements. Vis Res 41:3597–3611
Melcher D, Morrone MC (2015) Nonretinotopic visual processing in the brain. Vis Neurosci 32:E017
Melcher D, Piazza M (2011) The role of attentional priority and saliency in determining capacity limits in enumeration and visual working memory. PLoS One 6:e29296
Miller GA (1956) The magical number seven, plus or minus two: some limits on our capacity for processing information. Psychol Rev 63:81–97
Miller JM, Anstis T, Templeton WB (1981) Saccadic plasticity: parametric adaptive control by retinal feedback. J Exp Psychol Hum Percept Perform 7:356–366
Munoz DP, Broughton JR, Goldring JE, Armstrong IT (1998) Age-related performance of human subjects on saccadic eye movement tasks. Exp Brain Res 121:391–400
Munuera J, Morel P, Duhamel J-R, Deneve S (2009) Optimal sensorimotor control in eye movement sequences. J Neurosci 29:3026–3035
Niemeier M, Crawford JD, Tweed DB (2003) Optimal transsaccadic integration explains distorted spatial perception. Nature 422:76–80
Niemeier M, Crawford JD, Tweed DB (2007) Optimal inference explains dimension-specific contractions of spatial perception. Exp Brain Res 179:313–323
Noto CT, Robinson FR (2001) Visual error is the stimulus for saccade gain adaptation. Cogn Brain Res 12:301–305
O’Regan JK, Lévy-Schoen A (1983) Integrating visual information from successive fixations: does trans-saccadic fusion exist? Vis Res 23:765–768
O’Regan JK, Noë A (2001) A sensorimotor account of vision and visual consciousness. Behav Brain Sci 24:939–973 Discussion 973–1031
Ohl S, Rolfs M (2017) Saccadic eye movements impose a natural bottleneck on visual short-term memory. J Exp Psychol Learn Mem Cogn 43:736–748
Ohl S, Rolfs M (2018) Saccadic selection of stabilized items in visuospatial working memory. Conscious Cogn 64:32–44
Ohl S, Brandt SA, Kliegl R (2013) The generation of secondary saccades without postsaccadic visual feedback. J Vis 13:11
Oostwoud Wijdenes L, Marshall L, Bays PM (2015) Evidence for optimal integration of visual feature representations across saccades. J Neurosci 35:10146–10153
Ostendorf F, Dolan RJ (2015) Integration of retinal and extraretinal information across eye movements. PLoS One 10:e0116810
Paeye C, Collins T, Cavanagh P, Herwig A (2018) Calibration of peripheral perception of shape with and without saccadic eye movements. Atten Percept Psychophys 80:723–737. https://doi.org/10.3758/s13414-017-1478-3
Pashler H (1988) Familiarity and visual change detection. Percept Psychophys 44:369–378
Pélisson D, Alahyane N, Panouillères M, Tilikete C (2010) Sensorimotor adaptation of saccadic eye movements. Neurosci Biobehav Rev 34:1103–1120
Pelli DG, Tillman KA (2008) The uncrowded window of object recognition. Nat Neurosci 11:1129–1135
Penny W (2012) Bayesian models of brain and behaviour. ISRN Biomath 785791:1–19. https://doi.org/10.5402/2012/785791
Peterson MS, Kramer AF, Irwin DE (2004) Covert shifts of attention precede involuntary eye movements. Percept Psychophys 66:398–405
Pollatsek A, Rayner K, Collins WE (1984) Integrating pictorial information across eye movements. J Exp Psychol Gen 113:426–442
Pollatsek A, Rayner K, Henderson JM (1990) Role of spatial location in integration of pictorial information across saccades. J Exp Psychol Hum Percept Perform 16:199–210
Poth CH, Schneider WX (2016) Breaking object correspondence across saccades impairs object recognition: the role of color and luminance. J Vis 16:1
Poth CH, Herwig A, Schneider WX (2015) Breaking object correspondence across saccadic eye movements deteriorates object recognition. Front Syst Neurosci 9:176
Prablanc C, Massé D, Echallier JF (1978) Error-correcting mechanisms in large saccades. Vis Res 18:557–560
Prime SL, Niemeier M, Crawford JD (2006) Transsaccadic integration of visual features in a line intersection task. Exp Brain Res 169:532–548
Prime SL, Tsotsos L, Keith GP, Crawford JD (2007) Visual memory capacity in transsaccadic integration. Exp Brain Res 180:609–628
Prime SL, Vesia M, Crawford JD (2011) Cortical mechanisms for trans-saccadic memory and integration of multiple object features. Philos Trans R Soc B 366:540–553
Prsa M, Thier P (2011) The role of the cerebellum in saccadic adaptation as a window into neural mechanisms of motor learning. Eur J Neurosci 33:2114–2128
Rayner K, Pollatsek A (1983) Is visual information integrated across saccades? Percept Psychophys 34:39–48
Rich D, Cazettes F, Wang Y et al (2015) Neural representation of probabilities for Bayesian inference. J Comput Neurosci 38:315–323
Richard AM, Luck SJ, Hollingworth A (2008) Establishing object correspondence across eye movements: flexible use of spatiotemporal and surface feature information. Cognition 109:66–88
Robinson F, Noto C, Watanabe S (2000) Effect of visual background on saccade adaptation in monkeys. Vis Res 40:2359–2367
Rolfs M, Carrasco M (2012) Rapid simultaneous enhancement of visual sensitivity and perceived contrast during saccade preparation. J Neurosci 32:13744–13752a
Ross J, Morrone MC, Goldberg ME, Burr DC (2001) Changes in visual perception at the time of saccades. Trends Neurosci 24:113–121
Schneider WX (2013) Selective visual processing across competition episodes: a theory of task-driven visual attention and working memory. Philos Trans R Soc Lond Ser B Biol Sci 368:20130060
Schut MJ, Fabius JH, der Stoep NV, der Stigchel SV (2017) Object files across eye movements: previous fixations affect the latencies of corrective saccades. Atten Percept Psychophys 79:138–153
Shao N, Li J, Shui R et al (2010) Saccades elicit obligatory allocation of visual working memory. Mem Cogn 38:629–640
Shebilske WL (1976) Extraretinal information in corrective saccades and inflow vs outflow theories of visual direction constancy. Vis Res 16:621–628
Siegelmann HT, Holzman LE (2010) Neuronal integration of dynamic sources: Bayesian learning and Bayesian inference. Chaos 20:037112
Souto D, Gegenfurtner KR, Schütz AC (2016) Saccade adaptation and visual uncertainty. Front Hum Neurosci 10:227
Sperling G (1960) The information available in brief visual presentations. Psychol Monogr Gen Appl 74:1–29
Strasburger H, Rentschler I, Jüttner M (2011) Peripheral vision and pattern recognition: a review. J Vis 11:13
Szinte M, Cavanagh P (2011) Spatiotopic apparent motion reveals local variations in space constancy. J Vis 11:4
Tas AC, Moore CM, Hollingworth A (2012) An object-mediated updating account of insensitivity to transsaccadic change. J Vis 12:18
Tas AC, Luck SJ, Hollingworth A (2016) The relationship between visual attention and visual working memory encoding: a dissociation between covert and overt orienting. J Exp Psychol Hum Percept Perform 42:1121–1138
Tatler BW, Land MF (2011) Vision and the representation of the surroundings in spatial memory. Philos Trans R Soc Lond Ser B Biol Sci 366:596–610
Tatler BW, Gilchrist ID, Rusted J (2003) The time course of abstract visual representation. Perception 32:579–592
Tian J, Ying HS, Zee DS (2013) Revisiting corrective saccades: role of visual feedback. Vis Res 89:54–64
van den Berg R, Shin H, Chou W-C et al (2012) Variability in encoding precision accounts for visual short-term memory limitations. Proc Natl Acad Sci 109:8780–8785
van Opstal AJ, van Gisbergen JAM (1989) Scatter in the metrics of saccades and properties of the collicular motor map. Vis Res 29:1183–1196
Wallman J, Fuchs AF (1998) Saccadic gain modification: visual error drives motor adaptation. J Neurophysiol 80:2405–2416
Warabi T, Kase M, Kato T (1984) Effect of aging on the accuracy of visually guided saccadic eye movement. Ann Neurol 16:449–454
Weber RB, Daroff RB (1972) Corrective movements following refixation saccades: type and control system analysis. Vis Res 12:467–475
Weiß K, Schneider WX, Herwig A (2015) A “blanking effect” for surface features: transsaccadic spatial-frequency discrimination is improved by postsaccadic blanking. Atten Percept Psychophys 77:1500–1506
Westheimer G (1954) Eye movement responses to a horizontally moving visual stimulus. AMA Arch Ophthalmol 52:932–941
Wexler M, Collins T (2014) Orthogonal steps relieve saccadic suppression. J Vis 14:13
Wheeler ME, Treisman AM (2002) Binding in short-term visual memory. J Exp Psychol Gen 131:48–64
Wittenberg M, Bremmer F, Wachtler T (2008) Perceptual evidence for saccadic updating of color stimuli. J Vis 8:9
Wolf C, Schütz AC (2015) Trans-saccadic integration of peripheral and foveal feature information is close to optimal. J Vis 15:1
Wolf W, Hauske G, Lupp U (1980) Interaction of pre- and postsaccadic patterns having the same coordinates in space. Vis Res 20:117–125
Wong AL, Shelhamer M (2011) Saccade adaptation improves in response to a gradually introduced stimulus perturbation. Neurosci Lett 500:207–211
Wurtz RH (2008) Neuronal mechanisms of visual stability. Vis Res 48:2070–2089
Zhang W, Luck SJ (2008) Discrete fixed-resolution representations in visual working memory. Nature 453:233
Zhang W, Chen A, Rasch MJ, Wu S (2016) Decentralized multisensory information integration in neural systems. J Neurosci 36:532–547
Acknowledgement
We thank Karl Gegenfurtner, Heiner Deubel, Martin Rolfs, Eckart Zimmerman, and Sebastian Schneegans for their helpful comments on a draft version of this manuscript. This work was supported by the Wellcome Trust (grant number 106926).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Aagten-Murphy, D., Bays, P.M. (2018). Functions of Memory Across Saccadic Eye Movements. In: Hodgson, T. (eds) Processes of Visuospatial Attention and Working Memory. Current Topics in Behavioral Neurosciences, vol 41. Springer, Cham. https://doi.org/10.1007/7854_2018_66
Download citation
DOI: https://doi.org/10.1007/7854_2018_66
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-31025-7
Online ISBN: 978-3-030-31026-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)