- Email: [email protected]
Almeria spatial memory recognition test (ASMRT): Gender differences emerged in a new passive spatial task
Neuroscience Letters 651 (2017) 188–191
Contents lists available at ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Research article
Almeria spatial memory recognition test (ASMRT): Gender differences emerged in a new passive spatial task Laura Tascón a , Luis Miguel García-Moreno b , Jose Manuel Cimadevilla a,∗ a b
Department of Psychology, University of Almeria, Spain Departmental Section of Psychobiology, Complutense University of Madrid, Spain
h i g h l i g h t s • A new recognition task discloses gender differences. • Task difficulty modulates dimorphism. • The simplicity of the task makes it a good candidate for screening studies.
a r t i c l e
i n f o
Article history: Received 6 March 2017 Received in revised form 25 April 2017 Accepted 7 May 2017 Available online 9 May 2017 Keywords: Dimorphism Hippocampus Spatial orientation Recognition task
a b s t r a c t Many different human spatial memory tasks were developed in the last two decades. Virtual reality based tasks make possible developing different scenarios and situations to assess spatial orientation but sometimes these tasks are complex for specific populations like children and older-adults. A new spatial task with a very limited technological requirement was developed in this study. It demanded the use of spatial memory for an accurate solution. It also proved to be sensitive to gender differences, with men outperforming women under high specific difficulty levels. Thanks to its simplicity it could be applied as a screening test and is easy to combine with EEG and fMRI studies. © 2017 Elsevier B.V. All rights reserved.
1. Introduction Spatial memory is an ability that permits human beings to orientate themselves through space and reach targets effectively. Nowadays, spatial memory is frequently studied using virtual reality-based tasks. Virtual reality allows the development of different environments, depending on the necessity of each study. Participants can adopt an active or a passive role during the spatial exploration. Therefore, they can play an active role if the task makes it possible an interaction between the participant and the environment. Under these circumstances, subjects could take decisions about paths and routes while compiling contextual information [1–3]. On the other hand, participants are sometimes demanded only to observe what is happening. Thus, they can take a passive role without interacting with objects or places [4–6]. This alterna-
∗ Corresponding author at: Department of Psychology, University of Almeria, Carretera de Sacramento s/n, 04120, Almería, Spain. E-mail addresses: [email protected] (L. Tascón), [email protected] (L.M. García-Moreno), [email protected] (J.M. Cimadevilla). http://dx.doi.org/10.1016/j.neulet.2017.05.011 0304-3940/© 2017 Elsevier B.V. All rights reserved.
tive reduces the technological demands of the task, thus being very suitable for people who are outdated or could have problems using new technologies. Recognition was frequently used to prove cognitive skills. Some neuropsychological visuospatial tests demand focusing on one scene or stimulus before making decisions about those stimuli in a recognition test. Hence, in the Spatial Cognitive Style test designed by Nori and Giusberti [7] participants have to recognize images of buildings or abstract symbols. Nevertheless, these tasks usually require object recognition but not place recognition since, as is generally known, place and objects are processed by different brain circuits [8,9]. Furthermore, spatial-memory-based tasks showed great sensitivity to medial temporal lobe disturbances, when traditional neuropsychological tests did not detect any problem [10]. It is worthy to note that gender differences frequently arise on spatial memory tasks, primarily under specific difficulty levels, thus not being usually registered under very low or very high task demands [4,11,12]. Since this dimorphism commonly appears in spatial memory tasks, it could be taken as an index of spatial memory demands, since this differentiation rarely appears in others visual tasks.
L. Tascón et al. / Neuroscience Letters 651 (2017) 188–191
Recently, the combination of video presentation and a spatial recognition task disclosed a differential performance between groups [13]. Nevertheless, in an attempt to create a spatial memory test in a format similar to traditional neuropsychological tests, the video presentation of the experimental environment was replaced by a room image. This study was aimed to develop a test based on a previous virtual reality-based task [11] sensitive to spatial memory abilities, useful for screening purposes in neuropsychology and easily compatible with brain activity studies as well. Different levels of difficulty were used by adding locations to be remembered. The order, increasing/decreasing, in the number of places to remember was also taken into account since it could modulate performance. Our prediction was that it would be easier to start with low difficulty in order to increase it gradually afterwards. Gender is here reported to be an important variable explaining performance in the task. 2. Material and method 2.1. Participants The sample was made up by 108 undergraduate students from the University of Almeria. They were divided into two groups balanced by gender: Increasing difficulty level, with 78 students (21.76 ± 4.38); and decreasing difficulty level, with 30 students (22.17 ± 3.43). Exclusion criteria included any circumstance that could potentially interfere with performance. This study was conducted in accordance with The Code of Ethics of the World Medical Association (Declaration of Helsinki) for experiments involving humans. 2.2. Apparatus The task was presented 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). 2.3. Procedure The Almeria Spatial Memory Recognition Test (ASMRT) was created with images from the original Boxes Room task [11]. The virtual room contains 9 brown boxes in three rows. A trial consisted of two phases: In the sample phase a picture of a virtual room full of boxes—all of them of brown colored but one of green— was displayed. Afterwards in the recognition phase, ten different pictures of the virtual room were presented one by one containing one green box and several brown boxes (see Fig. 1). Participants had to decide if the green box shown in the recognition image is located in the same position as in the sample picture. Half of the pictures were correct. Pictures were selected according to their informative value showed in previous studies [4,6]. Participants provided
189
affirmative responses whether the location of the green box was correct or answered negatively if it was wrong. Responses were registered manually by the experimenter avoiding pressure over response time. Students were given ten seconds during which they had to memorize the sample photo. No time limit was imposed in their responses during the recognition phase, although it took less than one minute per trial (ten pictures). Hence, one, two, and three green boxes were used in the sample picture to create three difficulty conditions. Nevertheless, all pictures contained only one green box in the recognition phase and they could show similar or different viewpoints in relation to the sample picture. At each level of difficulty four trials were implemented. As a way to determine how the previous experience could interfere with the difficulty, one group completed the task in an increasing order of the difficulty (one, two and three positions to remember) and another group in a decreasing order (three, two and one positions). 2.4. Statistical analyses Analyses were executed with the statistical package STATISTICA − version 7. Mean number of correct answers in each condition was analyzed applying a three-way ANOVA (Gender x Order x Difficulty) with repeated measures in the last variable. A Tukey test was applied for post-hoc comparisons. Differences were considered significant for p < 0.05.
3. Results An ANOVA (Gender x Order x Difficulty, with repeated measures in the last variable) revealed a significant main effect of Gender F(1,104) = 12.60, p < 0.05 (mean number of correct answers 37.34, SD = 0.56 and 34.57, SD = 0.53 for men and women, respectively) and Difficulty F(2,208) = 52.26, p < 0.001 (mean number of correct answers 38.2, SD = 0.38; 35.38, SD = 0.49 and 34.27, SD = 0.47 for one, two and three positions, respectively) but no effect of Order factor F(1,104) = 1.88, p > 0.05. Interactions Order x Difficulty F(2208) = 30.69, p < 0.001 and Gender x Difficulty F(2208) = 5.34, p < 0.05 were found statistically significant, but neither Gender x Order F(1,104) = 0.017, p > 0.05 nor Gender x Order x Difficulty interactions F(2, 208) = 1.38, p > 0.05. Post-hoc analysis of the interaction Order x Difficulty revealed that in the increasing order, participants obtained higher scores when it came to memorize three positions (mean number of correct answers 35.71, SD = 4.82 and mean 32.26, SD = 3.86 for increasing and decreasing conditions, respectively, p < 0.001; see Fig. 2). Post-hoc analysis of the interaction Gender x Difficulty revealed that men outperformed women when they were to memorize two or three spatial positions (mean number of correct answers in two green boxes condition 37.56, SD = 3.49 and mean 33.85, SD = 5.23 for men and women, respectively, p < 0.001; mean number of cor-
Fig. 1. Representation of the Almeria Spatial Memory Recognition Test (ASMRT). (A) Sample phase. A sight of the room is shown with one box in green. Participants have to memorize the location of this box. (B) A picture of the recognition phase. Participants have to decide if the colored box is located in the same position as in the sample image. In this example the box is in an incorrect location. (C) Another example of the recognition phase. Now the green box occupies the correct location. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
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L. Tascón et al. / Neuroscience Letters 651 (2017) 188–191
Fig. 2. Total number of correct answers by order and difficulty. Participants were better in recognizing three spatial positions when the order was direct from 1 to 3 locations. Mean ± SEM.
rect answers in three locations condition 36.37, SD = 3.9 and 33.88, SD = 5.23 for men and women, respectively, p < 0.05; see Fig. 3).
4. Discussion Our aim was to develop a new memory task where participants had to recognize spatial positions. Spatial memory tasks were shown to be more sensitive to hippocampal alterations than traditional neuropsychological tests. Hence, whereas spatial memory tasks disclosed group differences, other neuropsychological tests such as 10/36 spatial recall test did not show such sensitivity [10]. So this approximation could provide powerful tasks for neuropsychological assessment. This study demonstrated that participants can acquire spatial information from a picture and this memory can be measured in a recognition task. In recent works spatial learning was combined with a spatial recognition task [6,13]. Both studies reported good group discrimination supporting the use of recognition as an accurate method for assessing spatial learning. In our study the task was simplified since the learning phase consisted of a picture presentation that had to be memorized by participants. This simplification makes possible the development of a spatial memory task that could be easily administered in a format similar to traditional neuropsychological tests.
It is noteworthy that although participants did not actively explore the environment they could apprehend from a single location many context features. This makes the task parallel to other classical spatial memory tasks used in rodent research like the Morris water maze [14]. In fact, the active version of this test, a virtual reality-based task, disclosed similar results to those of the virtual Morris water maze in the same sample of subjects, showing both tools better discrimination than other tests [2]. In this study, instead of having a navigational experience like in other tests [6,13], a room picture was presented. In order to solve the task, participants had to build a mental map taking into account distal cues available. During the recognition phase, pictures showed a viewpoint of the virtual room. Since images were taken from a first person point of view, not all the walls and room landmarks were included in every picture. Accordingly, the ability to imagine a new viewpoint is crucial to solve this task. Therefore, only understanding the space and being able to have a flexible mental relation between the cues available would make an accurate solution possible [15]. On the other hand, this test was also sensitive to sexually dimorphic performance since men outperformed women, mainly with increasing difficulty conditions. Male subjects outperformed their female counterparts when they had to recognize two or three spatial positions, that is to say, when the task has certain level of difficulty. In a previous study, Tascón et al. [13] asked participants to
Fig. 3. Total number of correct answers by men and women. Men outperformed women when they had to memorize two and three spatial positions. Mean ± SEM.
L. Tascón et al. / Neuroscience Letters 651 (2017) 188–191
watch some videos about the spatial position of green boxes in a virtual room. A recognition test was used afterwards. Different grades of rotation in relation to the viewpoint were used. With big rotations gender differences appeared since task increased demands. A better spatial representation of the virtual room was required to obtain more complex viewpoint transformations. The working memory demands could also explain this differential outcome [16]. Hence studies by Coluccia & Louse [16] men outperformed women only with high visuospatial working memory load. Another factor influencing performance is the order of increasing or decreasing level of difficulty. Independently of gender, performance was poorer when the task started with the higher difficulty level. By contrast, participants obtained better scores if they had already passed the lower difficulty level. Under these testing conditions participants were more familiarized with the context and more capable to construct a flexible mental map [17]. Different brain areas are related to spatial memory and many different processes could be involved in this specific behavior. It is supposed that the hippocampus system is required when managing viewpoint-independent representations. As reported before, hippocampal lesions alter spatial memory across changes in viewpoint [18]. What is more, patients with refractory temporal lobe epilepsy were impaired in recognizing locations in a spatial memory task [6]. Nevertheless, other brain structures could also be involved during task performance. Thus, spatial updating associated to movement of viewpoint is mediated by parieto-occipital sulcus and retrosplenial cortex, probably serving the translation between egocentric and allocentric representations [15]. In addition, although their task maintains some differences with respect to the one we used, other brain structures participated in learning sequences of positions in two versions of the Corsi block tapping test. Hence, many cortical areas like the right lingual gyrus, angular gyrus, inferior and middle frontal gyrus, calcarine sulcus and dorsolateral prefrontal cortex would be important in learning in a navigational space [19]. Obviously the specific task demands would determine recruitment of other brain networks. Finally, sexual dimorphism could have its neural base in brain structures that show a differential activation during perspective image comprehension. Hence, males showed higher brain activation in right inferior frontal gyrus and precuneus than females [20,21]. 5. Conclusions Since spatial memory tasks were shown to be more sensitive to hippocampal disturbances, this approximation could provide important tools in neuropsychology research. Furthermore, the ASMRT test can be easily and rapidly applied in medical consultants without complex procedures or apparatus and this feature makes the task suitable for brain imaging studies.
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Acknowledgements ˜ for his help with English. We would like to thank Jose R. Ibanez This investigation was supported by MINECO (PSI2015-67442P) and by the Ministry of Education, Culture and Sport of Spain [FPU2013/02655]. References [1] R. Astur, A.J. Purton, M.J. Zaniewski, J.M. Cimadevilla, E.J. Markus, Human sex differences in solving a virtual navigation problem, Behav. Brain Res. 308 (2016) 236–243. [2] R. Cánovas, I. León, M.D. Roldán, R. Astur, J.M. Cimadevilla, Virtual reality tasks disclose spatial memory alterations in fibromyalgia, Rheumatology 48 (2009) 1273–1278. [3] E.A. Maguire, R. Nannery, H.J. Spiers, Navigation around London by a taxi driver with bilateral hippocampal lesions, Brain 129 (2006) 2894–2907. [4] L. Tascón, I. León, J.M. Cimadevilla, Viewpoint-related gender differences in a spatial recognition task, Learn. Individ. Differ. 50 (2016) 270–274. [5] S. Lambrey, M.A. Amorim, S. Samson, M. Noulhiane, D. Hasboun, S. Dupont, M. Baulac, A. Berthoz, Distinc visual perspective-taking strategies involve the left and right medial temporal lobe structures differently, Brain 131 (2008) 523–534. [6] K. Rosas, I. Parrón, P. Serrano, J.M. Cimadevilla, Spatial recognition memory in a virtual reality task is altered in refractory temporal lobe epilepsy, Epilepsy Behav. 28 (2013) 227–231. [7] R. Nori, F. Giusberti, Predicting cognitive styles from spatial abilities, Am. J. Psychol. 119 (2006) 67–86. [8] J. Bachevalier, S. Nemanic, Memory for spatial location and object-place associations are differently processed by the hippocampal formation, parahippocampal areas TH/TF and perirhinal cortex, Hippocampus 18 (2008) 64–80. [9] A.R. Preston, H. Eichenbaum, Interplay of hippocampus and prefrontal cortex in memory, Curr. Biol. 23 (2013) R764–R773. [10] J.M. Cimadevilla, J.R. Lizana, M.D. Roldán, R. Cánovas, E. Rodríguez, Spatial memory alterations in children with epilepsy of genetic origin or unknown cause, Epileptic. Disord. 16 (2014) 203–207. [11] R. Cánovas, M. Espínola, L. Iribarne, J.M. Cimadevilla, A new virtual task to evaluate human place learning, Behav. Brain Res. 190 (2008) 112–118. [12] I. León, J.M. Cimadevilla, L. Tascón, Developmental gender differences in children in a virtual spatial memory task, Neuropsychology 28 (2014) 485–495. [13] L. Tascón, I. León, J.M. Cimadevilla, Viewpoint-related gender differences in a spatial recognition task, Learn. Ind. Diff. 50 (2016) 270–274. [14] T. Wolbers, J.M. Wiener, Challenges for identifying neural mechanisms that support spatial navigation: the impact of spatial scale, Front. Hum. Neurosci. 8 (2014) 571, http://dx.doi.org/10.3389/fnhum.2014.0057. [15] S. Lambrey, C. Doeller, A. Berthoz, N. Burgess, Imaging being somewhere else: neural basis of changing perspective in space, Cereb. Cortex 22 (2012) 166–174. [16] E. Coluccia, G. Louse, Gender differences in spatial orientation: a review, J. Environ. Psychol. 24 (2004) 329–340. [17] T. Iachini, F. Ruotolo, G. Ruggiero, The effects of familiarity and gender on spatial representation, J. Environ. Psychol. 29 (2009) 227–234. [18] D.M. Parslow, R.G. Morris, S. Fleminger, Q. Rahman, S. Abrahams, M. Recce, Allocentric spatial memory in humans with hippocampal lesions, Acta Psychol. 118 (2005) 123–147. [19] F. Nemmi, M. Boccia, L. Piccardi, G. Galati, C. Guariglia, Segregation of neural circuits involved in spatial learning in reaching and navigational space, Neuropsychologia 51 (2013) 1561–1570. [20] S. Kaiser, S. Walther, E. Nenning, K. Kronmüller, C. Mundt, M. Weisbrod, C. Stippich, K. Vogeley, Gender-specific strategy use and neural correlates in a spatial perspective taking task, Neuropsychologia 46 (2008) 2524–2531. [21] S. Semrud-Clikeman, J.G. Fine, J. Bledsoe, D.C. Zhu, Gender differences in brain activation on a mental rotation task, Int. J. Neurosci. 122 (2012) 590–597.
Contents lists available at ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Research article
Almeria spatial memory recognition test (ASMRT): Gender differences emerged in a new passive spatial task Laura Tascón a , Luis Miguel García-Moreno b , Jose Manuel Cimadevilla a,∗ a b
Department of Psychology, University of Almeria, Spain Departmental Section of Psychobiology, Complutense University of Madrid, Spain
h i g h l i g h t s • A new recognition task discloses gender differences. • Task difficulty modulates dimorphism. • The simplicity of the task makes it a good candidate for screening studies.
a r t i c l e
i n f o
Article history: Received 6 March 2017 Received in revised form 25 April 2017 Accepted 7 May 2017 Available online 9 May 2017 Keywords: Dimorphism Hippocampus Spatial orientation Recognition task
a b s t r a c t Many different human spatial memory tasks were developed in the last two decades. Virtual reality based tasks make possible developing different scenarios and situations to assess spatial orientation but sometimes these tasks are complex for specific populations like children and older-adults. A new spatial task with a very limited technological requirement was developed in this study. It demanded the use of spatial memory for an accurate solution. It also proved to be sensitive to gender differences, with men outperforming women under high specific difficulty levels. Thanks to its simplicity it could be applied as a screening test and is easy to combine with EEG and fMRI studies. © 2017 Elsevier B.V. All rights reserved.
1. Introduction Spatial memory is an ability that permits human beings to orientate themselves through space and reach targets effectively. Nowadays, spatial memory is frequently studied using virtual reality-based tasks. Virtual reality allows the development of different environments, depending on the necessity of each study. Participants can adopt an active or a passive role during the spatial exploration. Therefore, they can play an active role if the task makes it possible an interaction between the participant and the environment. Under these circumstances, subjects could take decisions about paths and routes while compiling contextual information [1–3]. On the other hand, participants are sometimes demanded only to observe what is happening. Thus, they can take a passive role without interacting with objects or places [4–6]. This alterna-
∗ Corresponding author at: Department of Psychology, University of Almeria, Carretera de Sacramento s/n, 04120, Almería, Spain. E-mail addresses: [email protected] (L. Tascón), [email protected] (L.M. García-Moreno), [email protected] (J.M. Cimadevilla). http://dx.doi.org/10.1016/j.neulet.2017.05.011 0304-3940/© 2017 Elsevier B.V. All rights reserved.
tive reduces the technological demands of the task, thus being very suitable for people who are outdated or could have problems using new technologies. Recognition was frequently used to prove cognitive skills. Some neuropsychological visuospatial tests demand focusing on one scene or stimulus before making decisions about those stimuli in a recognition test. Hence, in the Spatial Cognitive Style test designed by Nori and Giusberti [7] participants have to recognize images of buildings or abstract symbols. Nevertheless, these tasks usually require object recognition but not place recognition since, as is generally known, place and objects are processed by different brain circuits [8,9]. Furthermore, spatial-memory-based tasks showed great sensitivity to medial temporal lobe disturbances, when traditional neuropsychological tests did not detect any problem [10]. It is worthy to note that gender differences frequently arise on spatial memory tasks, primarily under specific difficulty levels, thus not being usually registered under very low or very high task demands [4,11,12]. Since this dimorphism commonly appears in spatial memory tasks, it could be taken as an index of spatial memory demands, since this differentiation rarely appears in others visual tasks.
L. Tascón et al. / Neuroscience Letters 651 (2017) 188–191
Recently, the combination of video presentation and a spatial recognition task disclosed a differential performance between groups [13]. Nevertheless, in an attempt to create a spatial memory test in a format similar to traditional neuropsychological tests, the video presentation of the experimental environment was replaced by a room image. This study was aimed to develop a test based on a previous virtual reality-based task [11] sensitive to spatial memory abilities, useful for screening purposes in neuropsychology and easily compatible with brain activity studies as well. Different levels of difficulty were used by adding locations to be remembered. The order, increasing/decreasing, in the number of places to remember was also taken into account since it could modulate performance. Our prediction was that it would be easier to start with low difficulty in order to increase it gradually afterwards. Gender is here reported to be an important variable explaining performance in the task. 2. Material and method 2.1. Participants The sample was made up by 108 undergraduate students from the University of Almeria. They were divided into two groups balanced by gender: Increasing difficulty level, with 78 students (21.76 ± 4.38); and decreasing difficulty level, with 30 students (22.17 ± 3.43). Exclusion criteria included any circumstance that could potentially interfere with performance. This study was conducted in accordance with The Code of Ethics of the World Medical Association (Declaration of Helsinki) for experiments involving humans. 2.2. Apparatus The task was presented 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). 2.3. Procedure The Almeria Spatial Memory Recognition Test (ASMRT) was created with images from the original Boxes Room task [11]. The virtual room contains 9 brown boxes in three rows. A trial consisted of two phases: In the sample phase a picture of a virtual room full of boxes—all of them of brown colored but one of green— was displayed. Afterwards in the recognition phase, ten different pictures of the virtual room were presented one by one containing one green box and several brown boxes (see Fig. 1). Participants had to decide if the green box shown in the recognition image is located in the same position as in the sample picture. Half of the pictures were correct. Pictures were selected according to their informative value showed in previous studies [4,6]. Participants provided
189
affirmative responses whether the location of the green box was correct or answered negatively if it was wrong. Responses were registered manually by the experimenter avoiding pressure over response time. Students were given ten seconds during which they had to memorize the sample photo. No time limit was imposed in their responses during the recognition phase, although it took less than one minute per trial (ten pictures). Hence, one, two, and three green boxes were used in the sample picture to create three difficulty conditions. Nevertheless, all pictures contained only one green box in the recognition phase and they could show similar or different viewpoints in relation to the sample picture. At each level of difficulty four trials were implemented. As a way to determine how the previous experience could interfere with the difficulty, one group completed the task in an increasing order of the difficulty (one, two and three positions to remember) and another group in a decreasing order (three, two and one positions). 2.4. Statistical analyses Analyses were executed with the statistical package STATISTICA − version 7. Mean number of correct answers in each condition was analyzed applying a three-way ANOVA (Gender x Order x Difficulty) with repeated measures in the last variable. A Tukey test was applied for post-hoc comparisons. Differences were considered significant for p < 0.05.
3. Results An ANOVA (Gender x Order x Difficulty, with repeated measures in the last variable) revealed a significant main effect of Gender F(1,104) = 12.60, p < 0.05 (mean number of correct answers 37.34, SD = 0.56 and 34.57, SD = 0.53 for men and women, respectively) and Difficulty F(2,208) = 52.26, p < 0.001 (mean number of correct answers 38.2, SD = 0.38; 35.38, SD = 0.49 and 34.27, SD = 0.47 for one, two and three positions, respectively) but no effect of Order factor F(1,104) = 1.88, p > 0.05. Interactions Order x Difficulty F(2208) = 30.69, p < 0.001 and Gender x Difficulty F(2208) = 5.34, p < 0.05 were found statistically significant, but neither Gender x Order F(1,104) = 0.017, p > 0.05 nor Gender x Order x Difficulty interactions F(2, 208) = 1.38, p > 0.05. Post-hoc analysis of the interaction Order x Difficulty revealed that in the increasing order, participants obtained higher scores when it came to memorize three positions (mean number of correct answers 35.71, SD = 4.82 and mean 32.26, SD = 3.86 for increasing and decreasing conditions, respectively, p < 0.001; see Fig. 2). Post-hoc analysis of the interaction Gender x Difficulty revealed that men outperformed women when they were to memorize two or three spatial positions (mean number of correct answers in two green boxes condition 37.56, SD = 3.49 and mean 33.85, SD = 5.23 for men and women, respectively, p < 0.001; mean number of cor-
Fig. 1. Representation of the Almeria Spatial Memory Recognition Test (ASMRT). (A) Sample phase. A sight of the room is shown with one box in green. Participants have to memorize the location of this box. (B) A picture of the recognition phase. Participants have to decide if the colored box is located in the same position as in the sample image. In this example the box is in an incorrect location. (C) Another example of the recognition phase. Now the green box occupies the correct location. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
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Fig. 2. Total number of correct answers by order and difficulty. Participants were better in recognizing three spatial positions when the order was direct from 1 to 3 locations. Mean ± SEM.
rect answers in three locations condition 36.37, SD = 3.9 and 33.88, SD = 5.23 for men and women, respectively, p < 0.05; see Fig. 3).
4. Discussion Our aim was to develop a new memory task where participants had to recognize spatial positions. Spatial memory tasks were shown to be more sensitive to hippocampal alterations than traditional neuropsychological tests. Hence, whereas spatial memory tasks disclosed group differences, other neuropsychological tests such as 10/36 spatial recall test did not show such sensitivity [10]. So this approximation could provide powerful tasks for neuropsychological assessment. This study demonstrated that participants can acquire spatial information from a picture and this memory can be measured in a recognition task. In recent works spatial learning was combined with a spatial recognition task [6,13]. Both studies reported good group discrimination supporting the use of recognition as an accurate method for assessing spatial learning. In our study the task was simplified since the learning phase consisted of a picture presentation that had to be memorized by participants. This simplification makes possible the development of a spatial memory task that could be easily administered in a format similar to traditional neuropsychological tests.
It is noteworthy that although participants did not actively explore the environment they could apprehend from a single location many context features. This makes the task parallel to other classical spatial memory tasks used in rodent research like the Morris water maze [14]. In fact, the active version of this test, a virtual reality-based task, disclosed similar results to those of the virtual Morris water maze in the same sample of subjects, showing both tools better discrimination than other tests [2]. In this study, instead of having a navigational experience like in other tests [6,13], a room picture was presented. In order to solve the task, participants had to build a mental map taking into account distal cues available. During the recognition phase, pictures showed a viewpoint of the virtual room. Since images were taken from a first person point of view, not all the walls and room landmarks were included in every picture. Accordingly, the ability to imagine a new viewpoint is crucial to solve this task. Therefore, only understanding the space and being able to have a flexible mental relation between the cues available would make an accurate solution possible [15]. On the other hand, this test was also sensitive to sexually dimorphic performance since men outperformed women, mainly with increasing difficulty conditions. Male subjects outperformed their female counterparts when they had to recognize two or three spatial positions, that is to say, when the task has certain level of difficulty. In a previous study, Tascón et al. [13] asked participants to
Fig. 3. Total number of correct answers by men and women. Men outperformed women when they had to memorize two and three spatial positions. Mean ± SEM.
L. Tascón et al. / Neuroscience Letters 651 (2017) 188–191
watch some videos about the spatial position of green boxes in a virtual room. A recognition test was used afterwards. Different grades of rotation in relation to the viewpoint were used. With big rotations gender differences appeared since task increased demands. A better spatial representation of the virtual room was required to obtain more complex viewpoint transformations. The working memory demands could also explain this differential outcome [16]. Hence studies by Coluccia & Louse [16] men outperformed women only with high visuospatial working memory load. Another factor influencing performance is the order of increasing or decreasing level of difficulty. Independently of gender, performance was poorer when the task started with the higher difficulty level. By contrast, participants obtained better scores if they had already passed the lower difficulty level. Under these testing conditions participants were more familiarized with the context and more capable to construct a flexible mental map [17]. Different brain areas are related to spatial memory and many different processes could be involved in this specific behavior. It is supposed that the hippocampus system is required when managing viewpoint-independent representations. As reported before, hippocampal lesions alter spatial memory across changes in viewpoint [18]. What is more, patients with refractory temporal lobe epilepsy were impaired in recognizing locations in a spatial memory task [6]. Nevertheless, other brain structures could also be involved during task performance. Thus, spatial updating associated to movement of viewpoint is mediated by parieto-occipital sulcus and retrosplenial cortex, probably serving the translation between egocentric and allocentric representations [15]. In addition, although their task maintains some differences with respect to the one we used, other brain structures participated in learning sequences of positions in two versions of the Corsi block tapping test. Hence, many cortical areas like the right lingual gyrus, angular gyrus, inferior and middle frontal gyrus, calcarine sulcus and dorsolateral prefrontal cortex would be important in learning in a navigational space [19]. Obviously the specific task demands would determine recruitment of other brain networks. Finally, sexual dimorphism could have its neural base in brain structures that show a differential activation during perspective image comprehension. Hence, males showed higher brain activation in right inferior frontal gyrus and precuneus than females [20,21]. 5. Conclusions Since spatial memory tasks were shown to be more sensitive to hippocampal disturbances, this approximation could provide important tools in neuropsychology research. Furthermore, the ASMRT test can be easily and rapidly applied in medical consultants without complex procedures or apparatus and this feature makes the task suitable for brain imaging studies.
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Acknowledgements ˜ for his help with English. We would like to thank Jose R. Ibanez This investigation was supported by MINECO (PSI2015-67442P) and by the Ministry of Education, Culture and Sport of Spain [FPU2013/02655]. References [1] R. Astur, A.J. Purton, M.J. Zaniewski, J.M. Cimadevilla, E.J. Markus, Human sex differences in solving a virtual navigation problem, Behav. Brain Res. 308 (2016) 236–243. [2] R. Cánovas, I. León, M.D. Roldán, R. Astur, J.M. Cimadevilla, Virtual reality tasks disclose spatial memory alterations in fibromyalgia, Rheumatology 48 (2009) 1273–1278. [3] E.A. Maguire, R. Nannery, H.J. Spiers, Navigation around London by a taxi driver with bilateral hippocampal lesions, Brain 129 (2006) 2894–2907. [4] L. Tascón, I. León, J.M. Cimadevilla, Viewpoint-related gender differences in a spatial recognition task, Learn. Individ. Differ. 50 (2016) 270–274. [5] S. Lambrey, M.A. Amorim, S. Samson, M. Noulhiane, D. Hasboun, S. Dupont, M. Baulac, A. Berthoz, Distinc visual perspective-taking strategies involve the left and right medial temporal lobe structures differently, Brain 131 (2008) 523–534. [6] K. Rosas, I. Parrón, P. Serrano, J.M. Cimadevilla, Spatial recognition memory in a virtual reality task is altered in refractory temporal lobe epilepsy, Epilepsy Behav. 28 (2013) 227–231. [7] R. Nori, F. Giusberti, Predicting cognitive styles from spatial abilities, Am. J. Psychol. 119 (2006) 67–86. [8] J. Bachevalier, S. Nemanic, Memory for spatial location and object-place associations are differently processed by the hippocampal formation, parahippocampal areas TH/TF and perirhinal cortex, Hippocampus 18 (2008) 64–80. [9] A.R. Preston, H. Eichenbaum, Interplay of hippocampus and prefrontal cortex in memory, Curr. Biol. 23 (2013) R764–R773. [10] J.M. Cimadevilla, J.R. Lizana, M.D. Roldán, R. Cánovas, E. Rodríguez, Spatial memory alterations in children with epilepsy of genetic origin or unknown cause, Epileptic. Disord. 16 (2014) 203–207. [11] R. Cánovas, M. Espínola, L. Iribarne, J.M. Cimadevilla, A new virtual task to evaluate human place learning, Behav. Brain Res. 190 (2008) 112–118. [12] I. León, J.M. Cimadevilla, L. Tascón, Developmental gender differences in children in a virtual spatial memory task, Neuropsychology 28 (2014) 485–495. [13] L. Tascón, I. León, J.M. Cimadevilla, Viewpoint-related gender differences in a spatial recognition task, Learn. Ind. Diff. 50 (2016) 270–274. [14] T. Wolbers, J.M. Wiener, Challenges for identifying neural mechanisms that support spatial navigation: the impact of spatial scale, Front. Hum. Neurosci. 8 (2014) 571, http://dx.doi.org/10.3389/fnhum.2014.0057. [15] S. Lambrey, C. Doeller, A. Berthoz, N. Burgess, Imaging being somewhere else: neural basis of changing perspective in space, Cereb. Cortex 22 (2012) 166–174. [16] E. Coluccia, G. Louse, Gender differences in spatial orientation: a review, J. Environ. Psychol. 24 (2004) 329–340. [17] T. Iachini, F. Ruotolo, G. Ruggiero, The effects of familiarity and gender on spatial representation, J. Environ. Psychol. 29 (2009) 227–234. [18] D.M. Parslow, R.G. Morris, S. Fleminger, Q. Rahman, S. Abrahams, M. Recce, Allocentric spatial memory in humans with hippocampal lesions, Acta Psychol. 118 (2005) 123–147. [19] F. Nemmi, M. Boccia, L. Piccardi, G. Galati, C. Guariglia, Segregation of neural circuits involved in spatial learning in reaching and navigational space, Neuropsychologia 51 (2013) 1561–1570. [20] S. Kaiser, S. Walther, E. Nenning, K. Kronmüller, C. Mundt, M. Weisbrod, C. Stippich, K. Vogeley, Gender-specific strategy use and neural correlates in a spatial perspective taking task, Neuropsychologia 46 (2008) 2524–2531. [21] S. Semrud-Clikeman, J.G. Fine, J. Bledsoe, D.C. Zhu, Gender differences in brain activation on a mental rotation task, Int. J. Neurosci. 122 (2012) 590–597.