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Variations in Crowding, Saccadic Precision, and Spatial Localization

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Variations in Crowding, Saccadic Precision, and Spatial Localization Variations in crowding, saccadic precision, and spatial PNAS PLUS localization reveal the shared topology of spatial vision John A. Greenwooda,1, Martin Szinteb, Bilge Sayimc,d, and Patrick Cavanaghe,f aExperimental Psychology, University College London, London WC1H 0AP, United Kingdom; bAllgemeine und Experimentelle Psychologie, Ludwig-Maximilians- Universität München, Munich 80802, Germany; cDepartment of Psychology, University of Bern, Bern 3012, Switzerland; dSciences Cognitives et Sciences Affectives (SCALab), CNRS UMR 9193, Université de Lille, Lille 59000, France; eLaboratoire Psychologie de la Perception, CNRS UMR 8242, Université Paris Descartes, Paris 75006, France; and fDepartment of Psychological and Brain Sciences, Dartmouth College, Hanover, NH 03755 Edited by David J. Heeger, New York University, New York, NY, and approved March 21, 2017 (received for review September 16, 2016) Visual sensitivity varies across the visual field in several characteristic extent than those along the tangential/iso-eccentric axis (9, 10). ways. For example, sensitivity declines sharply in peripheral (vs. These variations may similarly reflect cortical magnification, given foveal) vision and is typically worse in the upper (vs. lower) visual the greater rate of change along the radial axis than along the field. These variations can affect processes ranging from acuity and tangential axis (11), although perhaps at a cortical locus beyond crowding (the deleterious effect of clutter on object recognition) to V1 (12). Crowded interference zones are also larger along the the precision of saccadic eye movements. Here we examine whether vertical than along the horizontal meridian (10, 13, 14) and in the these variations can be attributed to a common source within the upper rather than the lower visual field (10, 15), with considerable visual system. We first compared the size of crowding zones with the variation between individuals (9, 10). precision of saccades using an oriented clock target and two adjacent Similar patterns are evident across a range of processes in spatial flanker elements. We report that both saccade precision and vision, consistent with a common source for these topological var- crowded-target reports vary idiosyncratically across the visual field iations. As noted above, an increase in stimulus eccentricity impairs with a strong correlation across tasks for all participants. Neverthe- performance for acuity (1) and grating resolution (4). Both the less, both group-level and trial-by-trial analyses reveal dissociations decline in eccentricity and radial/tangential anisotropy have also COGNITIVE SCIENCES that exclude a common representation for the two processes. We been found for the discrimination of phase (16) and orientation (17) PSYCHOLOGICAL AND therefore compared crowding with two measures of spatial locali- and for localization tasks such as Vernier acuity and bisection (5, 18, zation: Landolt-C gap resolution and three-dot bisection. Here we 19). Eye movements are similarly affected — both the distribution observe similar idiosyncratic variations with strong interparticipant of landing errors for saccadic eye movements (20) and the detection correlations across tasks despite considerably finer precision. Hierar- of position shifts in saccadic targets (21) show these characteristics. chical regression analyses further show that variations in spatial Additionally, as with crowding, performance is worse in the upper precision account for much of the variation in crowding, including the correlation between crowding and saccades. Altogether, we than in the lower visual field for gap resolution and Vernier acuity demonstrate that crowding, spatial localization, and saccadic preci- (22, 23), along with a range of other spatial identification measures sion show clear dissociations, indicative of independent spatial rep- (24, 25) that similarly show worse performance along the vertical resentations, whilst nonetheless sharing idiosyncratic variations in than the horizontal meridian. spatial topology. We propose that these topological idiosyncrasies The simplest explanation for these common patterns of vari- are established early in the visual system and inherited throughout ation would be that they arise from the same retinotopic map of later stages to affect a range of higher-level representations. the visual field. For the diverse range of spatial tasks listed peripheral vision | crowding | saccadic eye movements | position | Significance spatial vision Our ability to see, localize, and interact with stimuli varies ur sensitivity to visual stimuli varies substantially across the depending on their location in the visual field. Here we con- Ovisual field with characteristic patterns that are evident sider the source of these variations for several aspects of spa- across a wide range of tasks. Most notably, our ability to see fine tial vision: crowding (the disruption of object recognition in detail decreases sharply as objects move into peripheral vision clutter), spatial localization, and saccadic eye movements. We (1). These abilities are further disrupted by crowding, the im- observe a range of variations across both individuals and the pairment of object recognition in clutter, which also increases visual field with strong correlations between all tasks. How- with eccentricity (2, 3). Both of these effects have been attributed ever, a number of dissociations exclude the possibility that to an overrepresentation of the fovea at the expense of periph- these correlations arise from the same spatial representation of eral vision, known as “cortical magnification” (4, 5), which has the visual field. Rather, we propose a “topology of spatial vision,” been observed in a range of retinotopically organized areas of whereby idiosyncratic variations in spatial precision are estab- the brain (6, 7). Here we ask whether other variations in visual lished early in the visual system and inherited up to the highest sensitivity can similarly be attributed to topological principles levels of object recognition and motor planning. within the visual system and consider whether these variations might share a common source. Author contributions: J.A.G., M.S., B.S., and P.C. designed research; J.A.G. and M.S. per- formed research; J.A.G. and M.S. analyzed data; and J.A.G., M.S., B.S., and P.C. wrote Variations across the visual field are particularly apparent with the paper. crowding, a process that presents the fundamental limitation on The authors declare no conflict of interest. object recognition in peripheral vision (8). Crowding disrupts the This article is a PNAS Direct Submission. recognition of a target object when flanker objects fall within a Freely available online through the PNAS open access option. “ ” surrounding interference zone. As well as increasing in size with 1To whom correspondence should be addressed. Email: [email protected]. eccentricity, these zones show an elliptical shape whereby flankers This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. along the radial axis from fixation cause crowding over a greater 1073/pnas.1615504114/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1615504114 PNAS Early Edition | 1of10 Downloaded by guest on October 2, 2021 above, this seems unlikely. For example, although performance saccades, we conducted a second experiment to compare crowding on Vernier tasks has clear links with cortical area V1 (26), as do with two “lower-level” measures of spatial localization: gap reso- variations in grating resolution (27), both can also be linked with lution and bisection thresholds. We observe strong correlations retinal variations (5). Crowding also shows neural correlates in between these spatial-localization measures and crowding, con- area V1 (28–30), although stronger links have been proposed sistent with a shared source of topological variations. Hierarchical with cortical area V2 (31), and neural modulations have been regression analyses further reveal that these lower-level correla- foundashighasareaV4(32)andbeyond(33).Distinctneural tions account for much of the shared variance between crowding correlates are perhaps more clear in the case of saccadic eye move- and saccadic precision. Altogether, our results are consistent with ments, which likely rely on a distinct retino-collicular pathway to the these spatial tasks resulting from dissociable processes that cortex, unlike the geniculo-striate route taken by signals for percep- nonetheless inherit their topological variations from a common tual localization (34). source. The common pattern of variations across the visual field may instead be due to shared topological properties in the spatial maps Results that underlie these processes. Given the hierarchical structure of the Experiment 1. We first compared the precision of saccades with the visual system, with inherited receptive field properties at each stage spatial extent of crowding in a dual-task paradigm. Participants (35), variations in this topological representation could arise early in were required to saccade to the center of a crowded clock target the visual system, with patterns specific to each individual that are and subsequently identify the orientation of its stroke (Fig. 1A). inherited throughout later stages. Alternatively, these similarities Twelve participants were tested with stimuli at two eccentricities may simply reflect common organizational principles (e.g., 36) that (4° and 8°) in each of the four
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