Vision Research 51 (2011) 323–332

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Vision Research

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Location and identity of targets ⇑ I-Fan Lin, Andrei Gorea

Laboratorie Psychologie de la , Paris Descartes University and CNRS, 45 rue des Saints Pères, 75006 Paris, France article info abstract

Article history: While the memory of objects’ identity and of their spatiotopic location may sustain transsaccadic spatial Received 4 August 2010 constancy, the memory of their retinotopic location may hamper it. Is it then true that perturb Received in revised form 17 October 2010 retinotopic but not spatiotopic memory? We address this issue by assessing localization performances of Available online 27 November 2010 the last and of the penultimate saccade target in a series of 2–6 saccades. Upon fixation, nine letter-pairs, eight black and one white, were displayed at 3° eccentricity around fixation within a 20° 20° grey Keywords: frame, and subjects were instructed to saccade to the white letter-pair; the cycle was then repeated. Iden- Spatial constancy tical conditions were run with the eyes maintaining fixation throughout the trial but with the grey frame Saccades moving so as to mimic its retinal displacement when the eyes moved. At the end of a trial, subjects Spatial memory Reference frame reported the identity and/or the location of the target in either retinotopic (relative to the current fixation 1 Object-identity memory dot) or frame-based (relative to the grey frame) coordinates. Saccades degraded target’s retinotopic loca- tion memory but not its frame-based location or its identity memory. Results are compatible with the notion that spatiotopic representation takes over retinotopic representation during eye movements thereby contributing to the stability of the visual world as its retinal projection jumps on our retina from saccade to saccade. Ó 2010 Elsevier Ltd. All rights reserved.

1. Introduction efficiency of these processes in stabilizing the visual world has been consistently challenged (see reviews by Cavanagh et al., 2010; Most visual tasks, from viewing natural scenes to reading this Deubel et al., 2002; Wurtz, 2008). article, require sequential inspection of an array of objects via sacc- The focal topic of the present study is spatiotopic (or reference- adic eye movements so that selected visual details can be resolved, frame-based) location coding and . Spatiotopic location identified, stored and retrieved. By so doing, however, saccades en- storage being independent of eye location should enhance the sta- tail a continuously jumping retinal projection of the world. The fact bility of the perceived world. Retinotopic location storage should that we do not experience its permanent jitter has been an endur- hinder it. Of course, the brain may store objects’ location in both ing scientific puzzle (see Burr & Morrone, 2010). reference frames but at some cost (sensory, , attentional, It has been proposed that the perceptual stability of the visual etc.). If such cost were to be avoided so as to favor world stability world is due to a number of jointly active processes such as retinal when the eyes move, preservation of spatiotopic memory should motion cancellation by proprioceptive signals and/or by an efferent prevail over retinal location mnemonic traces. In fact, one may copy (Bridgeman, 1995; Dodge, 1990; Helmholtz, 1867; Holst & conjecture that spatiotopic memory might even be enhanced dur- Mittelstaedt, 1971 (1950); Sperry, 1950; Stark & Bridgman, 1983), ing eye-movements compared to fixation conditions where retino- saccadic suppression (e.g. Bridgeman, Hendry, & Stark, 1975; Burr, topic coordinates suffice to localize objects in the world. Morrone, & Ross, 1994; Dodge, 1990; Matin, 1974; Volkmann, One form of transsaccadic spatiotopic storage is what has been Schick, & Riggs, 1968), reafferent visual information (Deubel, 2004; referred to as ‘transsaccadic fusion’, namely the correct transsacc- Deubel & Schneider, 1994; Deubel, Schneider, & Bridgeman, 1996, adic visual ‘pasting’ of parts of the same visual object separately 2002) including optic flow (Gibson, 1966), remapping (Cavanagh, presented before and after the saccade (e.g. Breitmeyer, Kropfl, & Hunt, Afraz, & Rolfs, 2010; Colby & Goldberg, 1999; Duhamel, Julesz, 1982; Jonides, Irwin, & Yantis, 1982; McConkie & Rayner, Bremmer, Ben Hamed, & Graf, 1997; Duhamel, Colby, & Goldberg, 1976). As experimentally defined, transaccadic fusion requires only 1992; Wurtz, 2008) and spatiotopic coding (Dodge, 1990; Holst & short-lived memory (the time of a saccade) but high spatial accu- Mittelstaedt, 1971(1950); Sperry, 1950). It remains that the racy that can be only achieved at the sensory level. In other words, transsaccadic fusion, if it exists, is likely to involve iconic rather than short term memory. It remains that the very existence of ⇑ Corresponding author. transsaccadic fusion has been repeatedly contested on methodo- E-mail address: [email protected] (A. Gorea). 1 In the context of this study ‘‘frame-based’’ and ‘‘spatiotopic’’ are equivalent terms logical (see Irwin, 1996) and theoretical (Rojer & Schwartz, 1990; and will be used interchangeably. Simons & Levin, 1997; Yeshurun & Schwartz, 1989) grounds and/

0042-6989/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.visres.2010.11.010 324 I-Fan Lin, A. Gorea / Vision Research 51 (2011) 323–332 or could not be replicated (DiLollo, 1980; Irwin, Yantis, & Jonidas, chosen based on preliminary trials so as to insure 100% identification 1983; Irwin, Zacks, & Brown, 1990; McConkie & Currie, 1996; at 3° eccentricity. O’Regan and Lévy-Schoen, 1983; Rayner & Pollatsek, 1983). Transsaccadic fusion is not the only form of spatiotopic storage 2.2. Procedure helpful in keeping track of where objects are in the world while moving the eyes. Relational information (whereby objects present Each trial started with the grey square-frame and its reticle across saccades are used as landmarks for post-saccadic localiza- displayed at the center of the screen and with the fixation bull’s tion updating; Deubel, 2004; Deubel & Schneider, 1994; Deubel eye displayed at a random position 1° away from the middle of the et al., 1996, 2002) stored at a coarser spatial scale (Cohen & Ivry, cross-reticle (Fig. 1A). Subjects were instructed to fixate the bull’s 1991; Irwin, 1996) and possibly at a more symbolic level involving eye black dot. Once the software detected a steady fixation for global shapes or schematic maps rather than refined stimulus 150 ms, the target (white letter-pair) and the eight distracters (black features (Aivar, Hayhoe, Chizk, & Mruczek, 2005; Hayhoe, letter-pairs) were simultaneously displayed around fixation (Fig. 1B Shrivastavah, Mruczek, & Pelz, 2003; Hochberg, 1968; Irwin, and F). They were turned off together with the fixation dot after 1996; Rensink, 2000) may still be useful in entertaining a stable 100 ms. Subsequently, subjects were presented with one out of perception of the world over durations larger than . two main stimulation sequences, a ‘saccade’ or a ‘fixation’ sequence. A rather drastic alternative to spatiotopic memory as a means of In the saccade blocks subjects were instructed to make saccades preserving spatial constancy is total post-saccadic of to the (white) targets as they appeared at different locations in a both spatio- and retinotopic pre-saccadic information (Horowitz series of 2–6 such changes. In this condition the grey frame and & Wolfe, 1998; Moore & Egeth, 1997; Wolfe, 1998; Wolfe, Klem- its reticle remained at their central position with respect to the pen, & Dahlen, 2000) or, empirically equivalent, the ‘non-represen- screen throughout the 2–6 target location (and identity) changes tation’ of such information (O’Regan, 1992; O’Regan and Noe, and thus throughout the 2–6 corresponding saccades. For the con- 2001; Rensink, 2000). Even though the notion of a perceptual dition where subjects had to report the location or identity of the world exclusively based on an ‘outside memory’ (O’Regan, 1992) last (i.e. 2nd) target (Fig. 1D) there were always two target changes is attractive, it has been consistently refuted by studies having (and hence two saccades). For the condition where subjects re- shown that such transsaccadic storage does exist (see above). ported the location or identity of the penultimate (i.e. respectively The rationale of the present study is based on the notion that 2nd–5th) target (Fig. 1B) the number of target changes was ran- storage of objects’ spatiotopic (or frame-based) location promotes domized across trials in-between 3 and 6 thus preventing subjects transsaccadic spatial constancy, while storage of their retinotopic from anticipating the end of a trial. On each saccade landing (as de- location hinders it. If so, spatiotopic location storage should be tected online; see below), a new fixation dot appeared within one more resistant to (or possibly even enhanced by) eye-movements raster frame at the location of the just extinguished target (namely than retinotopic location storage. Whether or not this is the case close by the current saccade landing position; Fig. 1C) together with is the main question asked in the present study. In addition, we the new letter-pairs (target and distracters) around and 3° away also inquire into the extent to which transsaccadic location storage from it (Fig. 1D). The location of the letter-pairs relatively to the fix- competes with object identity storage, a topic never addressed to ation dot was always the same. The new fixation dot, target and our knowledge. distracters were offset after 100 ms and the cycle repeated (Fig. 1 illustrates a cycle of two saccades and two frame shifts only). 2. Methods In the fixation blocks, subjects were instructed to fixate the bull’s eye throughout the trial. The bull’s eye, target and distracters 2.1. Stimuli were also offset 100 ms after their onset, with the grey frame and its reticle remaining at their current position for a duration equal Participants were seated in a completely dark room with the to the average saccade latency (as determined for each subject in head positioned on a chin rest, 63 cm from a 38° 28° 22W preliminary trials). Following this duration, the grey frame and Formac ProNitron 22800 screen with a spatial resolution of 1024 its reticle were shifted by 3° in a direction opposite to the target by 768 pixels and a 96 Hz refresh rate. Movements of the right position relative to the bull’s eye (orange arrow in Fig. 1G) so as eye were measured using an EyeLink 1000 Desktop Mount (SR to mimic the movement on the retina in the saccade blocks. This Research, Osgoode, Ontario, Canada) with an average spatial reso- movement was programmed as a sequence of four jumps over a to- lution of 0.25°, and a 1 kHz sampling rate. The experiment was tal duration of 50 ms (the average time of a saccade). Once the grey controlled by an Apple Dual Intel-Core Xeon computer; manual re- frame reached its new location, a new set of target and distracters sponses were recorded via a standard keyboard and mouse. The appeared around the immobile fixation dot at their initial positions experimental software controlling the stimuli display and response (with respect to the screen but not to the grey frame; Fig. 1H). As in recording was implemented in MATLAB (MathWorks, Natick, Mas- the saccade blocks, localization or identity reports of the last target sachusetts, USA), using the Psychophysics (Brainard, 1997; Pelli, were always made in a sequence of two letter-pairs presentations 1997) and EyeLink toolboxes (Cornelissen, Peters, & Palmer, 2002). (and two frame shifts), while reports of the penultimate target were Stimuli were letter-pairs2 (arial font 20, 0.73° 0.73°) randomly made for presentation sequences (and frame shifts) of 3–6. chosen from 20 consonants (Q, W, R, T, P, S, D, F, G, H, J, K, L, Z, X, C, V, At the end of each saccade or fixation trial and whatever the B, N, and M) on each trial. One white letter-pair (6.96 cd/m2) served (position or identity) task, the fixation dot changed its color as the target, and eight black letter-pairs (0.01 cd/m2) served as to red for 150 ms, after which the grey frame was shifted (within distracters. The nine letter-pairs were equally spaced (2.05° of visual one raster frame) to a new pseudo-random location with the size angle) 3° away from fixation (a 0.3° radius bull’s eye) and were dis- and direction of the shift constrained so that one of the nine re- played within a 20° 20° grey frame (1.36 cd/m2) partitioned in sponse boxes (randomly chosen) appeared at the spatiotopic loca- four equal quadrants by a black cross-like reticle (0.01 cd/m2; line tion of the relevant (last or penultimate) target in either the width: 0.07°; see Fig. 1). The background outside the grey frame retinotopic or spatiotopic location recall blocks (Fig. 1K and L; or- was black (0.01 cd/m2). The size and contrast of the letters were ange and green arrows show the gray frame shifts with respect to its previous position in E and I, respectively; note that as the 2 Presentation of single letters entailed 100% letter identity recall whatever the location of the letter-pairs relative to the fixation dot never chan- experimental condition. ged, this proviso was futile for the retinotopic recall task. Given I-Fan Lin, A. Gorea / Vision Research 51 (2011) 323–332 325

Fig. 1. Spatiotemporal layout of one trial involving the last two saccades in the Saccade-Fixed frame condition (A–E and J, K or L) or the two frame shifts in the Fixation- Moving frame conditions (A, F–I and J, K or L) trial. (In the actual ‘penultimate target’ experiments the number of saccades or frame shifts varied randomly in-between 3 and 6.) In both conditions, a trial started with an bull’s eye fixation dot (A) followed by a 100 ms presentation of eight black (distracters) and of one white (target) letter-pairs displayed on an invisible (shown here for illustration purposes), 3° radius circle around fixation (B and F). In the ‘saccade’ condition, observers had to saccade to the white (target) letter-pair (white arrows in B and D; in this illustration B shows the penultimate target and saccade) which was replaced upon detection of the saccade landing by a new fixation dot (C) followed within one raster frame by a new set of distracters and target (D; last target and saccade); in the ‘fixation’ condition, saccades were replaced by equivalent shifts of the grey frame indicated by the orange arrows in G and H with the fixation dot (G) and letter-pairs around it (H) appearing after intervals matched to the saccade condition. Note that in the absence of eye-movements the fixation dot and letter-pairs did not change position with respect to the screen (black rectangle) throughout the whole trial. At the end of the saccade or frame shift sequence, the fixation dot turned red (E and I) and, depending on the task, subjects were presented within the next raster frame with (i) either nine grey boxes around their current fixation only one of which occupied the retinal (blue boxes) or spatiotopic location (yellow boxes) of the last (K) or penultimate (L) target (localization task), or (ii) 18 consonants displayed on two rows of nine each including one letter of the target letter-pair (J; identification task). In all three cases (J–L), the grey frame underwent a final shift whose size was constrained so that one, randomly chosen response boxe be at the correct spatiotopic location (with equivalent shifts used in both retinotopic and identification recall tasks). The green and orange arrows in K and L indicate the grey frame shifts relative to the last frame of the ‘saccade’ (E) and ‘fixation’ (I) conditions, respectively. The spatial layouts are not at scale. that spatiotopic and retinotopic locations are mirror symmetric of a trial subjects had to retrieve it with respect to the current with respect to fixation, this final grey frame shift was meant to location of the grey frame. prevent observers from inferring one from the other in the last tar- In the target identification blocks, 18 out of the 20 possible con- get recall blocks. For homogeneity, final frame shifts were applied sonants were displayed in two rows of nine different letters above to all other experimental conditions. and below fixation (Fig. 1J). The letters and their order were In all experimental blocks involving a localization task, the pseudo-randomized across trials so that the top and bottom rows shift of the grey frame was immediately (one raster frame) fol- contained respectively the first and second letter of the target lowed by the presentation of nine grey squares (0.88° 0.88°) letter-pair. Subjects were told so and had to click on these two displayed around the current fixation with the same layout as letters. Separate blocks were run where subjects had to report on the letter-pairs. Only one of these squares coincided with target’s a random basis either the location (50%) or the identity of the retinotopic or spatiotopic position (blue and yellow boxes, respec- target (referred hereafter as the dual-task). The response-type tively, in Fig. 1K and L). Subjects made their (retinotopic or spa- was revealed at the end of each trial by the display of either the tiotopic) localization response by clicking on one of the nine localization squares or the two rows of letters.3 Response times boxes. The retinotopic position of a target was defined with re- spect to the fixation dot at the moment when this target was pre- 3 Note that the forced choice response format used here for all tasks allows the sented; at the end of a trial subjects had to retrieve it with direct comparison of the corresponding performances in d0 units. At least, this should respect to the current fixation dot. The spatiotopic position of a be the case according to Signal Detection Theory, that provides transformation tools 0 target was defined with respect to the grey frame (and its yoked from % correct to d whatever the number of forced choice alternatives. Such direct comparisions were not possible in previous studies most of which measured reticle) at the moment when this target was presented; at the end localization dispersion and percent correct identification. 326 I-Fan Lin, A. Gorea / Vision Research 51 (2011) 323–332

(the time interval between the onset of the ‘location squares’ or of subject. Given that a d0 derivation from a 81AFC procedure may look the letters and subject’s mouse click) were also recorded (even awkward, percent correct identification performances have also though subjects received no response speeding instruction). been transformed into their arcsine and processed as such in the There were altogether 20 experimental conditions as defined by: statistical analysis. Response times (RTs) from the onset of the (1) the target to be memorized (last or penultimate; hereafter response boxes or letters to subject’s click on one of them were also referred to as distinct experiments), (2) eye-movement behavior measured and processed statistically. (saccade or fixate), (3) task type specified by the memorization instructions (single-tasks: retinotopic or spatiotopic localization 3.2. Sensitivity (d0) or target identity; dual-tasks: retinotopic localization and target identity or spatiotopic localization and target identity) (see Table 1). Fig. 2 displays localization (left panels) and identification (right At the beginning of each ‘last’ or ‘penultimate’ target block, sub- panels) performances for the last (top) and penultimate (bottom) jects received one of five instructions, namely to memorize (last or target experiments under fixation and saccade conditions. Solid penultimate) target’s retinotopic or spatiotopic location, or its and open symbols are for single- (localization or identification) identity, or both target’s retinotopic location and identity, or tar- and dual-tasks (localization and identification). Circles and trian- get’s spatiotopic location and identity. gles denote retinotopic and frame-based localization perfor- All subjects got familiarized with each of the 20 different exper- mances, or identification performances in the corresponding imental conditions during 4–5 training hours. One subject (out of dual-tasks. Saccades appear to deteriorate retinotopic localization seven) was discarded based on her close to chance performance performance (by about 0.3 d0-units) and enhance by about as much in a number of conditions after 5 h of training. Each ‘single-task- (although this enhancement fails to reach statistical significance; last-target’ condition consisted of 96 trials run in two blocks of see below) frame-based localization performance be they assessed 48 trials (see Table 1). Each ‘dual-task-last-target’ condition con- in single- or dual-task conditions. Instead, saccades do not seem to sisted of 192 trials run in four blocks of 48 trials. Out of the total affect identification performances whether in the single- or dual- 28 last-target blocks, 14 (7 ‘saccade’ and 7 ‘fixation’) were run at task. Dual- (compared to single-) task conditions appear to deteri- the mid-term of the whole experimental period and the other 14 orate mostly spatiotopic localization (but the statistical analysis at the end of this period. The order was randomized across subjects. below also shows a significant drop in the identification of the pen- Subjects ran 120 trials for each ‘single-task-penultimate-target’ ultimate target). Finally, both localization and identification of the condition (in 5 blocks of 24 trials) and 240 trials for each ‘dual- last target are 1.2 d0-units better than of the penultimate target. task-penultimate-target’ condition (in 10 blocks of 24 trials). The This is understandable given memory fading (see Bays & Husain, 70 penultimate-target blocks were split into 10 sessions of 7 blocks 2008) and because the respective performances have been ob- (of 24 trials) with the order of the single and dual conditions tained under critically different conditions (fixed vs. randomized randomized across sessions and observers. Subjects were run in number of targets per trial; see Section 2). sessions of 1–3 h a day with breaks every half hour or whenever they Two three-way ANOVAs for the localization data (factors: eye- felt tired for a total of 9–12 days distributed over two to 3 weeks. movements, EM (fixate, saccade), reference frame, RF (retinotopic, frame-based), task type, TT (single, dual)) and two two-way ANO- 2.3. Subjects VAs for the identification data (factors EM and TT) separately per- formed for the ‘last’ and ‘penultimate target’ experiments5 confirm Six participants (three females; age range 21–38) completed the most of the observations above. Identification performances were full experimental set. They all had normal or corrected-to-normal expressed in both d0 and arcsin (%-correct) units with equivalent sta- vision and gave their informed consent. The experiments were car- tistical outcomes; only the d0 analysis is given below. (a1) Last sac- ried out according to the ethical standards laid down in the Decla- cades – localization: only the TT factor shows a significant effect ration of Helsinki. (F(1, 5) = 9.83, p = 0.0258) with the RF factor close to significance (F(1, 5) = 3.84, p = 0.10). Partial comparisons show that the dual-task affects spatiotopic localization but only marginally retinotopic 3. Results localization (spatiotopic: F(1, 5) = 9.94, p = 0.0253; retinotopic: F(1, 5) = 4.75, p = 0.0811). The interaction between factors EM and 3.1. Data analysis RF is not statistically significant (F(1, 5) = 3.27, p = 0.130), although a partial comparison shows a marginal EM effect for the retinotopic Eye movements were analyzed online to assess fixations, sac- localization (F(1, 5) = 4.27, p = 0.0938). (a2) Last saccades – identifica- cade onsets and landing positions. The eyes were said to fixate as tion: the two-way ANOVA shows no effect of either of the two factors long as the position of the tracked eye was within a radius of and no significant interaction (all p values > 0.18). (a3) Penultimate 1.5° about the fixation dot for at least 150 ms. A saccade was said saccades – localization: here again the only significant factor is TT to occur (and its trajectory was tracked to the next landing posi- (F(1, 5) = 9.20, p = 0.029), with the RF factor coming close to signifi- tion) when eye’s velocity exceeded 30°/s. A saccade was considered cance (F(1, 5) = 5.25, p = 0.07). This time both EM TT to come to an end once eye velocity dropped below 30°/s. Trials (F(1, 5) = 51.65, p = 0.0008) and EM RF (F(1, 5) = 9.1, p = 0.0295) were discarded if saccade latency exceeded 500 ms or if subjects interactions are highly significant. The EM TT interaction is mostly could not stabilize their eye position within the 1.5°-window over due to the fact that the dual-task entails a significant spatiotopic 500 ms. In the ‘fixation’ blocks, trials were discarded if observer’s (F(1, 5) = 37.87, p = 0.0016) but not retinotopic localization perfor- eyes left the 1.5°-window around the fixation dot before the grey mance drop. The EM RF interaction is mostly due to the fact that frame shift. Discarded trials were reinserted at the end of a block. saccades entail a significant drop of the retinotopic localization 0 0 Both localization and identity performance is given in d units. d performance (F(1, 5) = 28.79, p = 0.003) with the observed rise in values were derived from the percent correct (see Macmillan & the spatiotopic localization performance failing to reach significance Creelman, 2005) obtained in the 9AFC localization trials and in the 81AFC ‘identity’ trials4 for each experimental condition and

5 There are least three ways in which these different experimental conditions 4 Observers had to choose two letters, each one out of a different group of nine differed thereby justifying separate statistical analyses. These reasons are detailed in letters. Hence the number of possible choices is 81. Section 4. I-Fan Lin, A. Gorea / Vision Research 51 (2011) 323–332 327

Table 1 All experimental conditions with number of trials per condition (bold digits) and per block (with number of blocks per condition given in italics).

Last target Penultimate target Saccade Fixation Saccade Fixation No. of saccades or of gray frame shifts per trial h 2 2 3–6 3–6 Memory tasks Single Retinotopic location of target 96 (48 2) 96 (48 2) 120 (24 5) 120 (24 5) Spatiotopic location of target 96 (48 2) 96 (48 2) 120 (24 5) 120 (24 5) Identity of target 96 (48 2) 96 (48 2) 120 (24 5) 120 (24 5) Dual Retinotopic location + identity of target 192 (48 4) 192 (48 4) 240 (24 10) 240 (24 10) Spatiotopic location + identity of target 192 (48 4) 192 (48 4) 240 (24 10) 240 (24 10)

ab

c d

Fig. 2. Mean localization (a and c) and identification (b and d) sensitivity (d0) measurements for the ‘last’ (a and b) and ‘penultimate target’ experiments. Filled and open symbols are for single and dual-tasks, respectively. Circles and triangles are for conditions involving retinotopic and spatiotopic localizations, respectively; squares are for the single identification task. Bars are ±1SE.

(p = 0.17). (a4) Penultimate saccades – identification: TT is the behavior (fixate or saccade) and of the localization type (retinotop- only factor yielding a close to significant effect (F(2, 10) = 3.94, ic or spatiotopic) should be the same as the pattern observed for p = 0.054). the corresponding sensitivity measurements (i.e. d0 and RT should correlate positively). Instead, Fig. 3 (same conventions as Fig. 2) 3.3. Reaction times (RTs) shows that median RTs correlate negatively with d0 (see Fig. 2) for all three dimensions studied (i.e. eye-movements, reference frame Even though observers were not asked to perform the localiza- and task type) in the localization task but only for the task type tion or identification tasks in a speeded mode (with all emphasis dimension in the identification task. As for the sensitivity data, put on response accuracy), their RTs remain informative about the dual-task yields globally worse performances (i.e. longer RTs) the relationship between retinotopic and frame-based localization than the single-task even though such drop appears to be negligi- coding/retrieving. The sensitivity drop and enhancement observed ble for the localization task in the ‘penultimate target’ experiment. in the saccade (relative to the fixation) conditions for the retino- Once again, the largest dual performance drop (i.e. RT increase) is topic and spatiotopic localizations, respectively, might simply re- observed for conditions involving the spatiotopic localization task. flect the well known speed-accuracy trade-off effect (e.g. Palmer, That observers are globally slower in the spatiotopic than in the Huk, & Shadlen, 2005). If so, the pattern of RTs as a function of eyes’ retinotopic localization task (by up to 220 ms) suggests that the 328 I-Fan Lin, A. Gorea / Vision Research 51 (2011) 323–332

a b

c d

Fig. 3. Median localization (a and c) and identification (b and d) RTs for the last (a and b) and penultimate target conditions. Same notations as in Fig. 2. Bars are ±1SE. former, at least in the present experimental format, involves an 3.4. Distribution of the localization responses additional retrieval process possibly checking spatial relationships (e.g. Deubel, Wolf, & Hauske, 1984; Irwin, McConkie, Carlson- Figs. 4 and 5 show histograms of observers’ retinotopic and spa- Radvansky, & Currie, 1994). tiotopic localization choices (out of the nine equally spaced loca- Once again, two three-way ANOVAs for the localization data tions at 3° eccentricity around fixation), respectively. The angular (factors EM, RF and TT) and two two-way ANOVAs for the identifi- difference from the correct location was computed as the differ- cation data (factors EM and TT) separately performed for the ‘last’ ence between the actual and correct answer azimuth, with the fix- and ‘penultimate target’ experiments (see Note 5 and Section 4) ation dot as a reference. Correct choices are shown at 0°. White and support most of the qualitative observations above. (a1) Last black bars are for fixation and saccade conditions, respectively. Top saccades – localization: only the TT factor shows a significant effect and bottom panels are for the ‘last’ and ‘penultimate target’ exper- (F(1, 5) = 16.33, p = 0.0099). Of critical interest, there is also a ten- iments, respectively. Data for single and dual conditions are shown dency for factors EM and RF to interact (F(1, 5) = 4.09, p = 0.09). in the left- and right-hand panels. The general observation is that (a2) Last saccades – identification: as above, only the TT factor the two locations closest to the target are reported slightly more shows a significant effect (F(1, 5) = 15.31, p = 0.0009) with signifi- frequently than those far away from it and that, in the ‘penultimate cantly longer RTs for the identification coupled with spatiotopic target’ experiment, the two locations on the response circle oppo- than with retinotopic localization (spatiotopic: F(1, 5) = 27.96, site to the target location (i.e. ±160° away from it on the response p = 0.0061; retinotopic: F(1, 5) = 5.06, p = 0.0742). (a3) Penultimate circle) tend to be chosen slightly more frequently than the inter- saccades – localization: none of the three factors shows a significant mediate locations. This being said, the distribution of the retino- effect but, as for the d0 data above, the EM RF interaction is sig- topic localizations errors is pretty flat. The implication is that nificant (F(1, 5) = 7.54, p = 0.0405). Also as for the d0 data, this inter- when observers do not remember the location of the target they action is mostly due to the fact that saccades entail a significant mostly guess. This should be expected given that two adjacent drop of the retinotopic localization performance (F(1, 5) = 18.00, locations in the present design were separated by 2.05° of visual p = 0.0081) with the visible mean spatiotopic localization RT short- angle, a distance well beyond the uncertainty range of a transsacc- ening failing to reach significance. (a4) Penultimate saccades – iden- adic spatial memory evidenced in previous studies (less than 1.4° tification: once again, only the TT factor yields a significant effect for saccades within a range of 6–10°; e.g. Collins, Rolfs, Deubel, & (F(2, 10) = 6.81, p = 0.0136) with significant differences between Cavanagh, 2009; Deubel, 2004; Karn, Moeller, & Hayhoe, 1997). single and dual-spatiotopic RTs (F(1, 5) = 7.0, p = 0.0456) but not Two 3-way ANOVAs (factors: eye-movements, reference frame between single and dual-retinotopic RTs. and task type) separately performed on the standard deviations I-Fan Lin, A. Gorea / Vision Research 51 (2011) 323–332 329

4. Discussion

1 1 The present study yields five general observations (i) saccades (compared to fixation conditions) deteriorate retinotopic memory and possibly enhance spatiotopic memory (even though this latter 0.5 0.5 effect fails to reach statistical significance); (ii) a dual- (compared to single-) localization/identification task mostly deteriorates spa- tiotopic localization and to some extent identification perfor- 0 0 mances; (iii) response times correlate negatively with localization -200 -100 0 100 200 -200 -100 0 100 200 performances hence excluding the possibility that the modulation of the latter by eye-movements and reference frame is accountable in terms of a speed-accuracy trade-off; (iv) response times are globally slower (by up to 220 ms) in the spatiotopic than in the 1 1 retinotopic localization task suggesting that the former involves sac fix an additional retrieval process; and finally (v) retinotopic localiza- tion errors are close to evenly distributed about the correct loca- 0.5 0.5 tion (with the exception of the two closest locations). The present research undoubtedly supports the existence of a transaccadic retinotopic and spatiotopic memory trace (see re- 0 0 views by Cavanagh et al., 2010; Deubel et al., 2002; Wurtz, -200 -100 0 100 200 -200 -100 0 100 200 2008). Hence, along with other studies (e.g. Dickinson & Zelinsky, 2007; McCarley, Wang, Kramer, Irwin, & Peterson, 2003; Peterson, Kramer, Wang, Irwin, & McCarley, 2001) including those on inhibi- Fig. 4. Distribution of retinotopic localization responses relative to the correct tion of return (Klein, 2000; Klein & MacInnes, 1999; Müller & von location (0°). White and black bars are for fixation and saccade conditions. Top and Mühlenen, 2000; Takeda & Yagi, 2000), the present data do not bottom panels are for the ‘last’ and ‘penultimate’ target experiments, and left and right panels are for single and dual-task conditions. Vertical lines are ±1SE. support previous claims of an amnesic visual search process (Gilchrist & Harvey, 2000; Horowitz & Wolfe, 1998; Wolfe et al., 2000), nor do they support the notion of a perceptual world exclu- sively based on an ‘‘outside memory’’ (i.e. no ‘‘internal representa- tion’’; O’Regan, 1992). It should be noted, however, that the issue of 1 1 a memoryless visual search remains contentious as results depend on a number of factors not always equated across such studies (covert vs. overt , persistence or removal of the searched 0.5 0.5 items, etc.; for a recent overview see Dickinson & Zelinsky, 2007). Also note that transsaccadic memory needs not and most likely does not exhibit the spatial acuity required for transsaccadic fusion 0 0 (see reviews by Cavanagh et al., 2010; Irwin, 1996; Rensink, 2000). -200 -100 0 100 200 -200 -100 0 100 200 The present technique where localization performance was as- sessed in terms of percent correct with a 9AFC method (nine equally spaced locations on a 3° radius circle) does not allow an accurate specification of localization accuracy in degrees of visual 1 1 angle (see below). sac The main present finding is the pernicious effect entailed by fix saccades on retinotopic but not on spatiotopic localization perfor- 0.5 0.5 mances. While this effect is about equal in size for last and penultimate saccade target reports, it reaches statistical signifi- cance only for the latter (see below). Compared to conditions where the eyes do not move (but the frame of reference does), 0 0 -200 -100 0 100 200 -200 -100 0 100 200 saccadic eye movements (with a physically stable frame of refer- ence) worsen retinotopic localization performances (a sensitivity drop of about 0.3 d0 units and a response time increase of about

Fig. 5. Distribution of spatiotopic localization responses relative to the correct 100 ms) but do not affect, or possibly even improve spatiotopic location (0°). All conventions are as for Fig. 4. localization performances even though this trend is not statisti- cally significant. Such relative improvement (if confirmed in future experiments) would ensue from the fact that acting upon objects in of the localization distributions in the ‘last’ and ‘penultimate tar- space requires their spatiotopic coding when the eyes move but get’ experiments show a significant (F(1, 5) = 10.37, p = 0.023) can be successfully accomplished based on their retinotopic loca- and close to significant (F(1, 5) = 4.83, p = 0.079) task type (single tion with an immobile eye. vs. dual) effect for the ‘last’ and ‘penultimate target’ experiments, Many previous experimental designs were such that they could respectively. The remaining two factors yield p-values in-between not differentiate between eye-centered and frame-based localiza- 0.17 and 0.96. However, as expected from the corresponding anal- tion performances. In such designs localization and/or identifica- ysis of the sensitivity data, the present ANOVA yields significant tion performances may (e.g. Gersch, Kowler, Schnitzer, & Dosher, TT RF (F(1, 5) = 23.49, p = 0.005) and EM RF (F(1, 5) = 9.42, 2009; Irwin, 1992; Lawrence, Myerson, & Abrams, 2004) or may p = 0.028) interactions, comparable to those observed for the sensi- not (e.g. Bays & Husain, 2008) depend significantly on whether tivity data. the eyes move or not. In the present case no such difference is 330 I-Fan Lin, A. Gorea / Vision Research 51 (2011) 323–332 observed when localization performances are averaged across the The pernicious saccade effect on retinotopic but not on spatio- eye- and frame-based tasks (see panels a, c of Figs. 2 and 3)on topic localization memory should contribute to stabilizing the vi- the assumption that observers give about equal weights to the sual world. This does not exclude the possibility that the two reference frames (e.g. McGuire & Sabes, 2009; Wong & Mack, deterioration by saccades of retinotopic location memory could 1981). simply be a byproduct of the tight link between saccade program- Even though, on visual inspection the eye-movement/reference ming and spatial (Pearson & Sahraie, 2003; frame interaction looks pretty much the same for reports of the Theeuwes, Belopolsky, & Olivers, 2009; Wurtz, 2008). Inasmuch penultimate and last target reports (compare Fig. 2a with c and as saccades are programmed in retinal coordinates that need to Fig. 3 a with c), it does not reach statistical significance for the lat- be continuously refreshed, so should be the memory of their ter. There are at least three reasons why the comparison between previous retinal coordinates (e.g. Lawrence et al., 2004; Liu, Yttri, the two experiments may not be warranted. First, the ‘last target’ & Snyder, 2010). Instead, transsaccadic preservation of spatiotopic experiment consisted in only two saccades so that observers had memory may reflect the sustained activity of ‘‘gain field’’ (or ‘‘real no uncertainty as to the target whose position and/or identity position’’) neurons in a number of extrastriate areas (see reviews was to be reported. As a consequence, observers had to store only by Andersen, 1989; Galletti & Fattori, 2002). Within such a frame- one target per trial with its memory trace unaffected by storing work, the fact that a measurable amount of retinotopic memory prior or subsequent targets. This was not the case for the ‘penulti- survives saccades by a considerable amount of time could be mate target’ experiment where the rank order of this target in a attributed to a lingering attentional trace (see Golomb, Pulido, series of 3-to-6 successive targets was randomized so that observ- Albrecht, Chun, & Mazer, 2010). ers had to store two successive targets refreshed up to four times Even though saccades affect differently retinotopic and spatio- per trial. Understandably, last target performances are up to about topic overall localization performances, no such difference is ob- 1.2 d0 units higher than penultimate target performances with the served between the respective distributions of localization errors. corresponding response times up to about 200 ms shorter. The ab- Their analysis (see Figs. 4 and 5) shows that, independently of sence of a statistically significant eye-movement/reference frame whether subjects perform a retinotopic or a frame-based memory sensitivity interaction for the ‘last target’ experiment may thus be task and of whether or not they move their eyes, most localization due, amongst others, to a sensitivity ceiling effect (as the reliability errors occur for the two locations flanking the correct one and of d0 values larger than 3–3.5 is poor). Second, it is nowadays admit- opposite to it (with respect to fixation). Overall, however, the dis- ted that saccade programming is yoked with an attentional process- tribution of localization errors is pretty flat implying that observ- ing enhancement at the location of the saccade target (e.g. Kowler, ers’ location storage/retrieval uncertainty is at most ±2.05° (the Anderson, Dosher, & Blaser, 1995; Schneider & Deubel, 1995). Be- visual angle separating two adjacent locations in the present de- cause saccades are directed toward the last target and away from sign) for either the retinotopic or frame-based task whether the the penultimate one, the memory of the former should be enhanced eyes move or not.6 and of the latter weakened. Finally, inasmuch as saccade program- Unlike location memory, identity memory is independent of ming is in retinotopic coordinates (but see Findlay & Walker, 1999; whether or not the eyes move (see also Lawrence et al., 2004; McGuire & Sabes, 2009; Wurtz, 2008), their conversion into spatio- Bay & Hussein, 2008). One previous study that showed otherwise topic ones may not be needed or performed if no further saccade is (but only for items far away from the saccade target) was designed to be programmed (e.g. Horaguchi & Sugino, 2008). This would be so that identity and location could not be disentangled (e.g. Irwin, the case for the last but not for the penultimate saccade in a series. 1992). It may thus be that previously observed identity memory In short, the memory of a last target has a special status that makes depletion was mainly due to localization errors. That object’s loca- it difficult to compare with any other target. Bays and Husain tion and identity are separately processed (coded and/or stored (2008) data show indeed a massive drop in recalling the penulti- and retrieved) is only partly sustained by the present data. While mate compared to the last visited target with a much more attenu- in most cases (with the exception of localization sensitivity for ated recall drop for more time remote visited targets. the last target and of the response times for the penultimate target) A direct comparison between retinotopic and spatiotopic global the statistical analyses show significant identity and location per- performances also raises issues of debate as they strongly depend formance depletion in the dual- (compared to the single-) task, on the experimental design. In the present experiments, saccade they also indicate that this depletion is observed for the spatiotopic targets were always 3° from fixation so that storage of the saccade but not retinotopic localization-identification coupling. Given the direction (but not amplitude) was sufficient for retrieving target’s additional observation that identity and spatiotopic memory are retinotopic but not frame-based coordinates (as the distance be- eye-movement independent while retinotopic memory is not, tween target and reference frame varied across saccades). The one may speculate that identity and retinotopic location are jointly use of the nine response-squares occupying the same relative posi- coded so that they do not compete for attentional resources (hence tions as the target and distracter letter-pairs (see Fig. 1) may have no penalty when coupled in a dual-task) but are stored separately also significantly boosted retinotopic localization performances. (hence differently affected by saccades; e.g. Hollingworth & This is so because the response-squares at the non-target locations Rasmussen, in press; Kahneman, Treisman, & Gibbs, 1992; could have been used as spatial landmarks (reference-object the- Pylyshyn, 1989; Treisman & Gormican, 1988; Treisman & Sato, ory; Deubel, 2004) for the retinotopic but not for the frame-based 1990; Wheeler & Treisman, 2002; Xu & Chun, 2006). Instead, location retrieval. Along this same line of argument, an enrichment spatiotopic location and object identity might be differently coded of the reference frame with additional spatial landmarks may have and stored (e.g. Curtis, 2006; Ester, Serences, & Awh, 2009; boosted the spatiotopic but not the retinotopic localization perfor- Ghorashi, Enns, Klein, & Di Lollo, 2010; Harrison & Tong, 2009; mances. In short, differences between retinotopic and spatiotopic Todd & Marois, 2004; Umeno & Goldberg, 2001) so that they would localization performances are stimulus and task-design dependent compete for attentional resources at the coding stage hence and have no specific meaning when considered by themselves. The critical observation, however, is that whatever the retinotopic 6 and spatiotopic performances in the absence of eye-movements, This upper bound is well beyond the typical accuracy range estimated with direct methods (e.g. Collins et al., 2009; Deubel, 2004; Karn et al., 1997) as it was saccades worsen retinotopic performances by, in average, almost constrained by the sparse layout of the nine location alternatives used in the present 0 1 d -unit and more than 200 ms response time relatively to spatio- study. In other words, the present method is such that the correct responses it topic performance (penultimate target experiments). measures include all mislocalizations within the typical spatial uncertainty range. I-Fan Lin, A. Gorea / Vision Research 51 (2011) 323–332 331 entailing storage/retrieval depletion. Be it as it may, the relation- Galletti, C., & Fattori, P. (2002). Posterior parietal networks coding visual space. In ship between location and identity coding and storage has been a H.-O. M. Karnath & A. D. G. Vallar (Eds.), The cognitive and neural bases of spatial neglect (pp. 59–69). Oxford, UK: Oxford University Press. matter of debate for almost three decades (see Treisman & Gersch, T. M., Kowler, E., Schnitzer, B. S., & Dosher, B. A. (2009). Attention during Gormican, 1988) and remains an unsolved research topic (see sequences of saccades along marked and memorized paths. Vision Research, Cavanagh et al., 2010). 49(10), 1256–1266. Ghorashi, S., Enns, J. T., Klein, R. 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