Prism Adaptation Influences Perception but Not Attention: Evidence from Antisaccades Tanja Nijboer, Anneloes Vree, Chris Dijkerman and Stefan Van Der Stigchel

386 Cognitive neuroscience and neuropsychology

Prism adaptation influences perception but not attention: evidence from antisaccades Tanja Nijboer, Anneloes Vree, Chris Dijkerman and Stefan Van der Stigchel

Prism adaptation has been shown to successfully participants as measured by the tasks used. NeuroReport alleviate symptoms of hemispatial neglect, yet the 21:386–389 c 2010 Wolters Kluwer Health | Lippincott underlying mechanism is still poorly understood. In this Williams & Wilkins. study, the antisaccade task was used to measure the NeuroReport 21: effects of prism adaptation on spatial attention in healthy 2010, 386–389 participants. Results indicated that prism adaptation did Keywords: antisaccade task, attention, landmark task, perception, prism not influence the saccade latencies or antisaccade errors, adaptation both strong measures of attentional deployment, despite Department of Experimental Psychology, Helmholtz Institute, Utrecht University, a successful prism adaptation procedure. In contrast to The Netherlands

visual attention, prism adaptation evoked a perceptual bias Correspondence to Dr Tanja Nijboer, Department of Experimental Psychology, in visual space as measured by the landmark task. We Universiteit Utrecht, Heidelberglaan 2, 3584 CS Utrecht, The Netherlands conclude that prism adaptation has a differential influence Tel: + 31 30 253 3572; fax: + 31 30 253 4511; e-mail: [email protected] on visual attention and visual perception in healthy Received 20 January 2010 accepted 25 January 2010

Introduction saccade latencies than prosaccade trials and that partici- Prism adaptation has been shown to be a successful pants frequently make an erroneous saccade to the target treatment for hemispatial neglect, for example Ref. [1]. It in antisaccade trials [12,13]. Correct performance on anti- consists of visuomotor adaptation to an exposure to wedge saccade trials requires at least two intact attentional pro- prisms. Despite these results of successful treatment, the cesses: (i) the ability to suppress a reflexive (exogenous) underlying mechanism of prism adaptation is still poorly saccade towards the visual stimulus and (ii) the ability to understood. As hemispatial neglect is generally associated generate a voluntary (endogenous) saccade in the opposite with an imbalance of visual attention across the visual direction. In this study, performance on the antisaccade field [2], one of the hypothesized effects of prism adapta- task before and after prism adaptation has been compa- tion in hemispatial neglect is a redistribution of attentio- red. If prism adaptation indeed influences the attentional nal resources in space [3,4]. One way to gain more insight deployment in visual space, differences will be observed into the mechanisms underlying prism adaptation is by in saccade latencies and the number of erroneous eye assessing the effects of adaptation in healthy partici- movements before and after prism adaptation. pants, for a review, see Ref. [5] on perceptual and atten- Besides the effects on visual attention, the influence of tional tasks. Some evidence suggests that prism adaptation prism adaptation on visual perception will be investigated influences the allocation of both voluntary and reflexive using the landmark task. Participants perform multiple spatial attentional resources in healthy participants [6–8]. landmark tests in which they are requested to judge whe- In contrast, results of both serial and parallel visual search ther a line was pretransected to the left or to the right of tasks in healthy participants showed no effects of prism its center [14,15]. Numerous studies have shown that adaptation on the distribution of attention in space [9]. prism exposure induces a bias in visual space perception In this study, we used saccadic eye movements to measure in healthy participants, as shown by the perceptual land- the effect of prism adaptation on spatial attention in mark task [14,16,17]. healthy participants. Saccadic eye movements are good indicators of spatial attention, as the preparation of an eye Methods movement is always associated with a shift in spatial atten- Participants tion to the location of the next eye movement [10,11]. Fifteen students [three males; 10 right handed; mean In this study, we have used the antisaccade task to age: 22.0 years (SD: 2.4)] participated in the experiment. measure the effect of prism adaptation on spatial atten- All had normal or corrected-to-normal visual acuity. They tion in healthy participants. During the antisaccade task, were naive to the purpose of the study. The study was participants either have to make a saccadic eye move- approved by the appropriate ethics committee. ment towards the appearing stimulus after stimulus onset (i.e. prosaccade trials) or a saccade in the opposite direc- Apparatus tion as quickly as possible (i.e. antisaccade trials) [12]. The stimuli were displayed on a laCie Electron Results typically show that antisaccade trials have longer 22-in Blue 3 CRT monitor (60 Hz, 1024 Â 768 pixels).

0959-4965 c 2010 Wolters Kluwer Health | Lippincott Williams & Wilkins DOI: 10.1097/WNR.0b013e328337f95f

Eye movements were recorded using an Eyelink 1000 the left of the true midpoint. Participants were told that system (SR Research Ltd., Mississauga, Ontario, Canada) none of the transection marks was at the midpoint of with a temporal resolution of 1 ms and a spatial resolution the line, and they were asked to indicate verbally whether of 0.021. the transection mark was closer to the right end or to the left end. The different trials were presented on sheets of Participants were tested individually in a dimly lit room paper that were positioned directly in front of the com- and were seated in front of the computer with their chin puter screen on which the antisaccade task was presen- in a chin rest. Participants viewed the monitor from a ted. The order of the presentation of the lines was distance of 57 cm in the antisaccade task. In the landmark randomized. test, the participant’s head was kept aligned with the body midline by the chin rest with a viewing distance of 35 cm. Prism adaptation As most research on prism adaptation in the normal Stimuli and procedure population has found behavioral effects with left-shifting, Each participant performed the landmark task three but not right-shifting prisms [6,7], left-shifting prisms times. First, each participant performed the landmark were used in this study. The prism goggles were fitted task before prism adaptation to determine the subjective with wide-field, prismatic lenses, creating an optical midline of the participant (‘preadaptation’). Second, shift of 151 to the left. The exposure period consisted of the landmark task was performed after prism adaptation making pointing responses during 10 min to visual targets to make sure that the participant was sufficiently adapted presented 101 to the right or left of the participant’s body after removing the prism goggles (‘postadaptation 1’). midline. During the prism exposure, participants were Third, the landmark task was performed again after the asked to point at a fast but comfortable speed; they could antisaccade experiment to make sure that the partici- see the target, the ‘second’ half of their pointing trajec- pants were still adapted during the antisaccade experi- tory and their terminal error. Their head was kept aligned ment (‘postadaptation 2’). The sequence of the blocks with the body’s sagittal axis by a chin rest [1]. View of was therefore as follows: first antisaccade task, first land- the starting position and the ‘first’ half of the point- mark task, prism adaptation, second landmark task, ing trajectory was blocked by a board held under the second antisaccade task, third landmark task. A chin rest participant’s chin to ensure the optimal development of was used for positioning the participants’ head during the the adaptation. whole procedure. For a successful prism adaptation procedure, a rightward Antisaccade task shift of 3 cm of the landing position was required (as Each trial began with the presentation of a colored central measured by a ruler) at the end of the adaptation period. fixation cross (1.01 Â 1.01) against a black background. A This was measured by asking the participant to focus ‘red’ cross indicated a prosaccade trial, in which partici- on one of the landing positions, then close one’s eyes pants had to look at the target once it appeared. When and make a pointing movement with closed eyes to this the cross was ‘green’, participants had to look in the location and leave one’s finger at the exact landing opposite direction of where the target appeared at an position. A board was held under the participant’s chin to equal distance from the central fixation cross (antisaccade prevent perception of the start position or the arm. For trial). After 1000 ms, the target (a gray circle of 2.01) two participants, the shift was less than 3 cm, hence, the appeared at a distance of 13.51 on the right or on the left prism adaptation procedure was repeated. of the central cross. The target appeared on the same horizontal axis as the central cross. The antisaccade task Analyses consisted of 100 trials. Participants performed 25 practice Antisaccade task trials during the first antisaccade task. When errors Saccade latency was defined as the interval between target occurred on half or more of the practice trials, the training onset and the initiation of a saccadic eye movement. Trials block was repeated. Antisaccade and prosaccade trials were excluded when the saccade latency was lower than were mixed. 80 ms or higher than 600 ms, or more than two and a half standard deviations away from the participant’s mean Landmark task latency. Trials in which no saccade or too small a saccade Fourteen black horizontal lines, 250 mm long and 1 mm (< 31) was made were eliminated as well. The endpoint of thick, each centered on a separate A4 sheet of white the first saccade had to have an angular deviation of less paper were used. Each line had been transected at differ- than 22.51 from the center of the target or the mirrored ent distances. Of these 14 lines, two were transected in target location. In the first case, the saccade was classified the center and 12 were asymmetrically transected: six at as a prosaccade; in the second case the saccade was distances of either 2, 4, or 6 mm to the right of the true classified as an antisaccade. In other situations, the saccade midpoint and six at distances of either 2, 4, or 6 mm to was not analyzed.

Saccade latencies were analyzed using analysis of variance preadaptation), there was no difference between the with stimulus location (left vs. right), task (antisaccade latencies of antisaccades to the targets presented left vs. prosaccade) and time (before vs. after adaptation) (M = 226 ms, SD = 35 ms) and right [M = 227 ms, SD = as within subject factors. Antisaccade errors (i.e. an eye 36 ms; t(14) = 0.23; P = 0.81]. Importantly, there was movement to the target on an antisaccade trial) were again no difference in postadaptation between targets analyzed using analysis of variance with stimulus location presented left (M = 212 ms, SD = 22 ms) and right (left vs. right) and time (before vs. after adaptation) as [M = 212 ms, SD = 30 ms; t(14) = 0.10; P = 0.91]. This factors. indicates that prism adaptation did not evoke a difference in the saccade latency of antisaccades. Landmark task The landmark task was analyzed by counting how many Antisaccade errors times a participant answered left or right when the tran- The mean error rate was 13.7% (SD = 10.9%). There section mark was in the middle or in the other direction as were no main effects of antisaccade errors on stimulus indicated by the participant. A perceptual bias in a certain location and time (F < 1). The interaction was not signi- direction is indicated by the difference between these two ficant (F < 1). numbers. This difference was computed such that a posi- tive number refers to a rightward bias (indicating that Landmark task the transection was on the left when it was in the middle In preadaptation, there was rightward bias in the land- or to the right). mark task (M = 0.60, SD = 1.59). This rightward bias was similar for left-handed and right-handed participants (the Results were analyzed using t-tests (preadaptation vs. mean bias for both groups was 0.60). The rightward bias postadaptation 1, preadaptation vs. postadaptation 2, and became even more stronger in the second landmark task postadaptation 1 vs. postadaptation 2). Only the transec- [first postadaptation test; M = 2.20, SD = 1.90; t(14) = tion marks at a distance of 2 or 4 mm left and/or right 4.77, P < 0.001]. The stronger rightward bias was still of the center were used, as there were no errors with observed in the third landmark task [M = 2.27, SD = a distance of 6 mm. 1.44; t(14) = 5.49, P < 0.0001]. There was no significant difference between the second and third landmark task Results [t(14) = 0.17, P = 0.87], indicating that participants were Antisaccade task still adapted during the third administration of the task. Overall, 7.4% of the trials were excluded on the basis of the exclusion criteria (2.3% on the basis of the latency, the remaining trials because of directional errors other Discussion than erroneous prosaccades). The aim of this study was to investigate whether prism adaptation influences attentional deployment in visual Saccade latency space in healthy participants. The results on the anti- No main effect was found on saccade latency for stimulus saccade task showed that prism adaptation did not in- location (F < 1), indicating that there was no difference fluence the saccade latencies or antisaccade errors. As both in latencies between stimuli that were presented to the saccade latencies and antisaccade errors are measures of left or right. A main effect of task was found [F(1,14) = attentional processes, this provides strong evidence that 93.31, P < 0.0001], with shorter latencies in the prosac- prism adaptation did not influence attentional deploy- cade task (M = 152 ms, SD = 30 ms) than in the anti- ment in the current task. Results on the perceptual saccade task (M = 219 ms, SD = 31 ms). A main effect landmark task did show a strong effect of prism adap- of time was found [F(1,14) = 5.84, P < 0.05]: overall tation, which is in line with earlier studies [14,16,17]. A saccade latencies in the preadaptation task were longer rightward shift was obtained in the landmark task in both (M = 191 ms, SD = 49 ms) than saccades in the post- postadaptation tests, which indicated that participants adaptation task (M = 180 ms, SD = 42 ms). This is inter- were still adapted during the second antisaccade task. preted as a general training effect. None of the interactions In contrast to the null results on the antisaccade task, we reached significance (all P > 0.10). showed in an earlier study [3] that prism adaptation to a To ascertain that there was no subtle effect of prism rightward prismatic shift improved leftward orientation of adaptation that could not be shown by the analyses attention following an endogenous, but not an exogenous, described above, we tested whether saccade latencies of cue in two neglect participants. We suggested that prism antisaccades preadaptation and postadaptation were adaptation ameliorates neglect by improving compensa- different to the left and the right. If prism adaptation tory processes of leftward voluntary orienting rather than has an effect, it should be lateralized, thus showing a by a fundamental change in attentional bias. Although beneficial effect to the left and that is observed only in this suggestion explains why prism adaptation did not the postadaptation trials. At the start of the task (i.e. influence the more ‘reflexive’ attentional processes (i.e.

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