Viewpoint-related gender differences in a spatial recognition task

LEAIND-01342; No of Pages 5 Learning and Individual Differences xxx (2016) xxx–xxx

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Viewpoint-related gender differences in a spatial recognition task Laura Tascón, Irene León, José Manuel Cimadevilla ⁎ Department of Psychology, University of Almeria, Carretera de Sacramento s/n, 04120, Spain

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Article history: Received 4 December 2015 Received in revised form 16 June 2016 Accepted 11 August 2016 Available online xxxx Keywords: Spatial memory Dimorphism Hippocampus Virtual reality

a b s t r a c t The efficacy of active virtual reality based tasks to measure spatial memory is well known. Sometimes, studies have used recognition tests to assess memory retrieval. This process requires comparing the sample image with the representation built in the brain about the experimental context. The perspective of the image presented could also have an important role during testing. In this study we develop a new spatial task based on videos and a spatial recognition test. Participants had to watch four videos where they had to remember one or three box locations. After, they had to decide whether or not any of the pictures shown in the spatial recognition task corresponded to correct spatial positions shown in the video. Images could be taken from similar or different viewpoints. Participants acquired the task in few trials and men performed better than women when deciding about spatial perspectives in the high demanding task. This approximation could be suitable for reducing the use of peripheral devices, decreasing the technological demands and simplifying the combination of other techniques like fMRI. © 2016 Elsevier Inc. All rights reserved.

1. Introduction Spatial orientation is a basic ability in many species. Knowledge about the location of resources or potential dangers contributes to improve survival. This information about the spatial relationships between places and objects is organized in our memory to be used during displacements in our surroundings. In recent years, virtual reality-based (VR) tasks were applied to study human spatial behavior. These tasks enable the study of this cognitive ability in very different scenarios like towns, buildings or even mazes where participants have to find or avoid places (Antonova et al., 2011; Astur, Ortiz, & Sutherland, 1998; Cánovas, Espinola, Iribarne, & Cimadevilla, 2008; Maguire, Nannery, & Spiers, 2006). Experience with VR contexts can be modulated by the active vs passive role of the subject during the learning phase. An active environment exploration favors spatial mapping (Plancher, Tirard, Gyselinck, Nicolas, & Piolino, 2012); but Von Stülpnagel and Steffens (2012) showed that landmark recognition is improved after passive navigation in nonfamiliar environments. Passive displacement through the context could also provide some advantages for specific groups. Older adults or people with low videogame experience could show initial problems to master some of the devices used for navigating in VR contexts. Accordingly, passive spatial tasks decrease task demands, thus facilitating assessment in old-adults and other populations with technological handicaps. ⁎ Corresponding author. E-mail address: [email protected] (J.M. Cimadevilla).

On the other hand, many studies have used recognition tests to assess memory retrieval (Latini-Corazzini et al., 2010; Rizk-Jackson et al., 2006; Rosas, Parrón, Serrano, & Cimadevilla, 2013; Rosenbaum et al., 2000). Subjects usually have to decide about the relationships between an image and the context visited during the learning phase. This process requires comparing the sample image with the representation built in the brain about the experimental context. This process can be influenced by the reference frame adopted during the acquisition phase (Kelly & McNamara, 2010) and could be modulated by the point of view of the image taken. Nori et al. (2015) showed that retrieval of a path was impaired if the point of view changed with respect to the learning phase. Hence, participants increased response latencies when the viewpoint between acquisition and retrieval was shifted (Diwadkar & McNamara, 1997; Nori et al., 2015). In addition, several studies showed female advantage in object location memory tasks (Hill et al., 1995; Lejbak, Vrbancic, & Crossley, 2009; McBurney, Gaulin, Devineni, & Adams, 1997; Rahman, Wilson, & Abrahams, 2003) although the metric structure of the spatial layout is better represented by men (Iachini, Sergi, Ruggiero, & Gnisci, 2005), and familiarity with the environment influences performance (Piccardi et al., 2011). How the viewpoint modulates the object location memory performance in both genders is still a matter of debate. The aim of this study was to create a spatial memory task reducing the technological demands or other biases caused by mobility problems such as impulsivity or reduced mobility. It combined a video presentation with a spatial recognition task to assess spatial memory. Conditions with similar vs different perspectives were used. Our results showed the task can be acquired in few trials, and it is sensitive to gender-related

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Please cite this article as: Tascón, L., et al., Viewpoint-related gender differences in a spatial recognition task, Learning and Individual Differences (2016), http://dx.doi.org/10.1016/j.lindif.2016.08.007

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performance when recognition images are taken from different viewpoints. 2. Material and methods 2.1. Participants The sample included 48 male (21.73 ± 0.58) and 48 female (21.18 ± 2.27) students of Psychology from the University of Almería. They were randomly divided into three groups according to the experimental conditions (see Table 1). Participants were administered a short questionnaire about medical history, age, manual preference, education, profession, sport/s and videogame experience. Exclusion criteria included histories of cerebrovascular disease, drug addiction, neurological and psychiatric illness. No participants were taking medications that could affect navigation performance. This study was conducted in accordance with the European Community Council Directive, 2001/20/EC for biomedical research involving humans. 2.2. Apparatus The boxes-room task was executed on a Hewlett Packard 2600-MHz notebook equipped with 3 GB of RAM and a 15.4 Thin Film Transistor (TFT) color screen (1920 × 1200 pixels). A set of videos were recorded with a subject navigating in first person through a virtual room from different starting points.

In addition, in the three-position configuration we worked with two levels of difficulty. The low level of difficulty involved using pictures with perspectives of the room similar to those of the videos. Photos were always taken from the same point of view so as to minimize the need for understanding the perspective (Fig. 1). On the other hand, in the high difficulty condition, pictures were taken from very different room angles. Accordingly, participants had to imagine the room and their different angles to understand the perspective of the image presented during the subsequent recognition test (Fig. 1). Regarding the one-position condition, pictures were taken from very different viewpoints. Participants were given both written and verbal instructions about how to proceed. Participants were instructed to memorize the position occupied by the green box. No information regarding useful strategies, the location of the green boxes, or any other feature of the experiment was provided. 2.4. Statistical analyses The number of correct answers in the one-reward condition was analyzed applying a two-way ANOVA (Gender × Trial, with repeated measures in the last variable). Tukey test was applied for post hoc comparisons. In the three-reward condition, the number of correct answers was analyzed applying a three-way ANOVA (Gender × Difficulty × Trial, with repeated measures in the last variable). Tukey test was applied for post hoc analyses. Analyses were carried out with the statistical package STATISTICA (version 7). Differences in which p b 0.05 were considered to be significant.

2.3. Video and spatial recognition task 3. Results The task is based on the Boxes Room task, described by Cánovas et al. (2008). The boxes room consisted of a virtual decorated square room (100 m2), in which 16 brown boxes were symmetrically distributed on the floor. Several stimuli disambiguated spatial locations, including a door, a window, and several pictures hanging on the walls. In this modified version of the task, participants did not perform a virtual reality task, but they watched four first person videos. Videos started from any of the four room walls, changing from one video to other; however the rewarded locations were always the same. This meant that participants could improve their cognitive map, since different perspectives were included in each video. Each video lasted 15 s and showed how an avatar interacted with the room boxes, which changed color to green upon interaction. Videos showed a restricted view of the room. The four different videos were played again after finishing the whole presentation, totaling eight trials (videos). Two different configurations of the room were used, with one and three positions (green boxes) to remember, respectively. Immediately after each video, participants were submitted to a spatial recognition test. The spatial recognition test included a set of 10 images. These pictures were always the same for all videos. Each picture contained several boxes, one of them painted green. Participants had to decide if the green box corresponded to any of the green boxes shown in the video or not. In five of the ten pictures, the highlighted box was correct. They provided verbal answer and there were no time limits during this test. Nevertheless, subjects needed 3– 4 s to answer.

3.1. Three locations Analysis of correct answers with ANOVA revealed a significant main effect of Gender F (1, 60) = 7.44, p = 0.008, Trial, F (7, 420) = 4.95, p = 0.000, and a significant interaction Gender × Difficulty F (1, 60) = 5.39, p = 0.023. No significant results were found in the Difficulty factor F (1, 60) = 0.46, p = 0.5 or in other interactions. Post-hoc analysis of Trial factor showed that the mean of correct answers in the first and second trial of both conditions was lower than the mean of correct answers for trials 6, 7 and 8, p b 0.05. This means that participants had been learning throughout the trial. A post hoc analysis of Gender × Difficulty interaction showed that males were more accurate than females in the difficult condition (mean 58.13, SD = 9.91 and 47.19, SD = 9.67 for men and women, respectively, p = 0.003) (Fig. 2 and Fig. 3). 3.2. One location ANOVA revealed a significant main effect of Trial factor F (7, 210) = 5.09, p = 0.000 and a significant effect of the interaction Trial × Gender F (7, 210) = 2.20, p = 0.035. No differences were found in Gender F (1, 30) = 1.32, p = 0.259. Post hoc analysis of the interaction Trial × Gender did not reveal gender differences in any of the trials (p N 0.05) (Fig. 4).

Table 1 Distribution of participants between different task conditions. Sample

1 Position

3 Positions – similar perspective

3 Positions - different perspective

Men (n = 48) Age Women (n = 48) Age

16 22.13 ± 2.57 16 23.69 ± 6.29

16 21.06 ± 3.26 16 19.25 ± 1.81

16 22.00 ± 4.90 16 20.56 ± 3.12

Please cite this article as: Tascón, L., et al., Viewpoint-related gender differences in a spatial recognition task, Learning and Individual Differences (2016), http://dx.doi.org/10.1016/j.lindif.2016.08.007

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Fig. 1. Example of two images from the spatial recognition test. A and B were taken from similar perspectives. Mental rotation demanded is minimal. C and D show the same box taken from different perspectives. Mental rotation is required.

4. Discussion In this work we assessed memory in men and women in a spatial recognition task. Participants had to make decisions about spatial locations of objects watched in four videos. Two levels of difficulty were used. The procedure and the four videos presented in the ‘similar’ and ‘different’ conditions were the same. In the ‘similar’ condition, pictures of the recognition test were taken from similar perspectives. Conversely, the ‘different’ condition was composed with pictures taken from very different views demanding a more accurate spatial representation of the room. We demonstrated that men and women differed, with men being more accurate than women during the recognition task under high spatial orientation demands. Male advantage in spatial memory tasks is well known, a topic reviewed in Coluccia and Louse (2004) and Lawton (2010). Many works run on humans and other species reliably confirm this fact (Astur et al., 1998; Cimadevilla et al., 1999; Dawson, 1972; Ge, Qi, Qiao, Wang, & Zhou, 2013; Lövdén et al., 2007). Nevertheless, object location memory is considered to show female advantage (Hassan & Rahman, 2007; Rahman et al., 2003; Spiers, Sakamoto, Elliott, & Baumann, 2008; Voyer, Postma, Brake, & Imperato-McGinley, 2007)

and females showed a better performance when they had to retrieve a path from a different point of view in a real environment (Nori et al., 2015). In our study, participants had to determine in a spatial recognition test whether the green box of the picture corresponded to any of the green boxes shown in the video. Cognitive processes involved recognizing the object in a particular position. This was also tested under two conditions, one of them demanding changing the point of view of the image. We observed that only when the point of view was very different in the several pictures used, a male advantage emerged. In the ‘similar’ condition, groups did not differ. This shows that object location memory is influenced by the viewpoint of the scenario where the object is located. Adopting a new perspective requires a good representation of the environment, retrieving from the memory the environmental layout necessary for successfully solving the recognition task. Previous studies already suggested a male superiority in a 3D environment (Spiers et al., 2008). In our case, 3D environment is used in all the conditions, but male advantage arose only when a shift in the viewpoint was considered. These results are in agreement with male superiority when a task involves taking a third person perspective (Kaiser et al., 2008), with males outperforming females in the speed of perspective transformation (Gardner, Sorhus, Edmonds, & Potts, 2012). An important issue

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Fig. 3. Mean number of correct answers in the spatial recognition test with images taken from similar perspectives. Males and females performed similarly. Mean ± SEM.

Please cite this article as: Tascón, L., et al., Viewpoint-related gender differences in a spatial recognition task, Learning and Individual Differences (2016), http://dx.doi.org/10.1016/j.lindif.2016.08.007

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Fig. 4. Mean number of correct answers in the one reward condition. Groups did not differ. Mean ± SEM.

to consider is the angle between the imagined view and the current view shown in the picture used in the spatial recognition test. As Michelon and Zacks (2006) reported, the difficulty of a perspectivetaking task increases with the angular distance. In our study it was impossible to accurately analyze this variable due to the nature of the materials used (four videos and ten pictures taken from different room points). It seems clear that the same task could be solved using different strategies, and previous works showed that men and women differed in their way of solving spatial tasks. The ‘similar’ version of this task demands paying attention to the position occupied by the green boxes, and the relation of these positions to the several landmarks which disambiguate the environment. As suggested by other researchers (Iachini et al., 2005), females used landmark-based information for solving spatial tasks. Accordingly, the ‘similar’ version of the task could be successfully solved using this strategy. On the other hand, the ‘different’ version demanded relating the green box to various landmark configurations. An accurate solution can be better obtained by a subject with a good metric representation of the context, a feature of men's performance (Iachini et al., 2005). Females are prone to use egocentric reference frames whereas males were more heterogeneous in their strategy, using more metric/allocentric strategies (Kaiser et al., 2008). Nevertheless, in our task this is speculative since subjects answered yes/no to ten images repeated eight times during the spatial recognition test and they did not have to explain strategies chosen. In addition, when the number of locations was reduced (one green box), performance did not differ in the spatial recognition test. ANOVA disclosed differences that were not supported by post-hoc analyses. We considered that there is only a tendency in men to outperform women, as can be seen observing errors on trials 1 and 2. Note that in the one-location condition, only images taken from several viewpoints were used. This means that the number of positions to be remembered was also influencing task performance. Hence, group differences disappeared when the cognitive load of the task decreased. This agrees with previous studies where gender differences appeared under specific conditions, and these conditions were related to the number of rewards to retrieve (Cánovas et al., 2008; León, Tascón, & Cimadevilla, 2014). It is important to point out that our task was based on the Boxes Room task, a VR-based task previously used for studying spatial memory. Participants have to navigate through a virtual room to find rewarded positions that have to be retrieved in the following trials (Cánovas et al., 2008). Features of the Boxes Room task made it possible to adapt the difficulty to the populations studied, avoiding floor and ceiling effects and improving the discrimination between groups (Cánovas et al., 2008; Cimadevilla, Lizana, Roldán, Cánovas, & Rodríguez, 2014; León et al., 2014; Sánchez-Horcajo, Llamas-Alonso, & Cimadevilla, 2015). In this study, the test demanded a passive observing strategy, watching videos and paying attention to the rewarded

positions. Like in the Boxes Room, difficulty was modified by increasing the number of boxes rewarded in the video. Although it is well known that active exploration improves recall of environmental features (Chrastil & Warren, 2013; Plancher et al., 2012), passive exploration provides some advantages. Different populations like people with reduced mobility, hyperactivity, or elder people could find difficulties to perform activities with a joystick or keyboard. In addition to this, passive exploration would make it possible to assess small groups at a time and this could be adequate for exploring the use of spatial memory tasks as screening tests. It may also facilitate the combination of behavioral and neuroimaging techniques like fMRI for future studies. Therefore, the use of videos leads to task simplification and even under these passive testing conditions, the task produced significant group discrimination in our study. At the brain level, it is well known that hippocampus is a crucial brain structure in spatial memory (O'Keefe & Nadel, 1978). Hence, hippocampal lesions caused spatial memory alterations (Aradillas, Libon, & Schwartzman, 2011; Astur, Taylor, Mamelak, Philpott, & Sutherland, 2002; Bianchini et al., 2014; Cánovas, León, Serrano, Roldán, & Cimadevilla, 2011; Cimadevilla, López, Nieto, Aguirre, & Fernández, 2009; Folley, Astur, Jagannathan, Calhoun, & Pearlson, 2010; Rosas et al., 2013) including performance in the Boxes Room task (Cánovas et al., 2011). In relation to the task used in our experiments, the hippocampal system seems to support a viewpoint-independent behavior (King, Burgess, Hartley, Vargha-Khadem, & O'Keefe, 2002), although some other brain structures also contribute to this function (Lambrey, Doeller, Berthoz, & Burgess, 2012). On the other hand, behavioral dimorphism observed suggests differences in brain activity and/or anatomy. The hippocampus was demonstrated to show dimorphic features in humans with different covariance between the hippocampus and other brain structures in a gender-related fashion (Persson et al., 2014). Thus, men and women activate the left hippocampus differently, and women activate the right parietal and right frontal cortex when navigating in a virtual environment (Grön, Wunderlich, Spitzer, Tomczak, & Riepe, 2000). Nevertheless, other brain structures like the precuneus and right inferior frontal gyrus displayed a differential activity in men and women when performing a third person perspective task (Kaiser et al., 2008). In conclusion, the combination of video and spatial recognition tests is an interesting way to assess spatial abilities, avoiding problems related to the use of VR technologies. Acknowledgements We thank Nobel Perdu for help with English. This work was supported by the Ministry of Economy and Competitiveness (Spain) [PSI201567442P] and cofounded by FEDER. References Antonova, E., Parslow, D., Brammer, M., Simmons, A., Williams, S., Dawson, G. R., & Morris, R. (2011). Scopolamine disrupts hippocampal activity during allocentric spatial memory in humans: An fMRI study using a virtual analogue of the Morris water maze. Journal of Psychopharmacology, 25(9), 1256–1265. Aradillas, E., Libon, D. J., & Schwartzman, R. J. (2011). Acute loss of spatial navigational skills in a case of a right posterior hippocampus stroke. Journal of the Neurological Sciences, 308(1–2), 144–146. Astur, R. S., Ortiz, M. L., & Sutherland, R. J. (1998). A characterization of performance by men and women in a virtual Morris water task: A large and reliable sex difference. Behavioural Brain Research, 93(1–2), 185–190. Astur, R. S., Taylor, L. B., Mamelak, A. N., Philpott, L., & Sutherland, R. J. (2002). Humans with hippocampus damage display severe spatial memory impairments in a virtual Morris water task. Behavioural Brain Research, 132(1), 77–84. Bianchini, F., Di Vita, A., Palermo, L., Piccardi, L., Blundo, C., & Guariglia, C. (2014). A selective egocentric topographical working memory deficit in the early stages of Alzheimer's disease: A preliminary study. American Journal of Alzheimer's Disease and Other Dementias, 29(8), 749–754. Cánovas, R., Espinola, M., Iribarne, L., & Cimadevilla, J. M. (2008). A new virtual task to evaluate human place learning. Behavioural Brain Research, 190(1), 112–118. Cánovas, R., León, I., Serrano, P., Roldán, M. D., & Cimadevilla, J. M. (2011). Spatial navigation impairment in patients with refractory temporal lobe epilepsy: Evidence from a new virtual reality-based task. Epilepsy & Behavior, 22(2), 364–369.

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Please cite this article as: Tascón, L., et al., Viewpoint-related gender differences in a spatial recognition task, Learning and Individual Differences (2016), http://dx.doi.org/10.1016/j.lindif.2016.08.007