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Ecological measures of everyday spatial memory – an overview of everyday spatial memory problems, factors of influence and assessment methods Sarah Plukaard (0254819) Utrecht University, the Netherlands Supervisors: Albert Postma & Maartje de Goede Helmholtz Institute, Utrecht University, the Netherlands Abstract This review considers the use of everyday spatial memory, everyday problems with spatial memory, the neurological and psychological causes of these problems, and methods that can be used to assess everyday spatial memory. Everyday spatial memory problems involve ‘getting lost’ or ‘forgetting where to find car keys’. Specific everyday spatial memory problems are categorized into groups based on whether the problems concern small or large scale, short or long term, and static or dynamic spatial memory. Current evidence about the effects of age, gender, neurological damage, visual impairments, stress and mood on spatial memory performance is reviewed. It appears that age and hippocampal damage are factors that may influence all listed everyday problems, whereas other factors such as visual impairments and mood may cause only specific spatial memory problems. Everyday spatial memory can be measured by means of surveys and questionnaires to obtain information from subjective reports. Experimental research on everyday spatial memory behaviour can be carried out in virtual environments (VEs) or in real world environments. The validity, advantages and disadvantages of surveys, VE and real environment studies are discussed. Based on the evidence provided by current studies and recent VE developments, we consider virtual reality as the most appropriate and valid method to study everyday spatial memory. 1 1. Introduction Spatial memory is used to encode, store and retrieve spatial information. This cognitive process is essential for simple everyday activities such as finding your way to the supermarket and subsequently knowing where to find the milk. Spatial memory includes the ability to remember the spatial layout of environments, to know how to travel from one place to another, to remember the locations of objects, to know your own location in the environment, to have knowledge about the general geographic environment, and knowledge about spatial arrangements of objects. It is a complex multidimensional process which includes a variety of components that help us to orient and act in space (cf. Kessels, De Haan, Kapelle & Postma, 2001; Postma, 2005). Almost all everyday actions require adequate spatial abilities and deficits in spatial memory may have great impact on the quality of life. Even a simple action such as picking up one object (e.g. a glass of water) requires spatial abilities: finding the object in space and judging the distance between the glass and you hand. In everyday life, spatial memory is applied in different environments, different situations and by different people with different spatial abilities. For instance, spatial memory declines with age resulting in different spatial behaviour in the environment by elderly people (e.g. Burns, 1999). Specific questions are: How is spatial memory performance influenced by emergency situations or threatening environments? Which problems do people with spatial memory impairments encounter in everyday life? Which problems occur to all people in everyday spatial environments? How can we improve spatial memory performance in different environments or different situations? To answer these questions or to direct future research into answering these questions, this review focuses on spatial memory in natural environments. The purpose of this review is to present an overview of different forms of spatial memory, problems in everyday spatial memory, neurological and psychological origins of these problems, different methods to measure spatial memory in the natural environment, and the validity of these methods. 2 1.1. Taxonomy of spatial memory As spatial memory is a complex function, different components of spatial memory can be described which are necessary for different everyday actions. For instance when traveling to the supermarket you need to know where to go (route learning) where you could rely on knowing when to go left or right until you end up at the supermarket (response learning) or on having a spatial layout of the neighborhood in your mind (cognitive map). Before you leave, you require knowing where you left your car keys (object-location memory) which could be located on top of the table to the left of (categorical coding) or 10 cm next to a magazine (coordinate coding). During the journey you constantly have to update spatial information in order to orient yourself (spatial working memory), you have to know where the supermarket is located relative to your own position (egocentric frame of reference) or, when you have to take a detour, where the supermarket is relative to e.g. the church (allocentric frame of reference). For the majority of everyday activities you require spatial working memory. Spatial working memory is part of working memory in general which is considered as a system with two components: a ‘phonological loop’ which holds auditory and speech-based information and a ‘visuo-spatial sketchpad’ which holds visual and spatial information. These (slave) components are under attentional control of a ‘central executive’, responsible for a.o. selective attention, inhibition, coordination and switching between stimuli, tasks and retrieval strategies (Baddeley, 1996; Baddeley, 1998). The visuo-spatial sketchpad which holds visual and spatial information thus includes spatial working memory. Spatial working memory on its own involves the ability to keep spatial information active for short periods of time in order to update or process this information (Jonides, Smith, Koeppe, Awh, Minoshima & Mintun, 1993; Van Asselen, 2005). In everyday life this form of spatial memory is required for all activities in which the environment is changing. For instance during a walk from one place to another (e.g. from your house to the supermarket) you require the ability to update spatial information with almost every step you take in order to keep track of where you are in space. Furthermore, in order to plan the route, you require holding spatial information active in memory so you can decide where to go next. 3 Traveling from one place to another does not just require spatial working memory, but is distinguished as a form of spatial memory on its own as route learning or spatial navigation (e.g. Postma, Jager, Kessels, Koppeschaar & Van Honk, 2004; Van Asselen, 2005). Route learning includes way finding and navigating in familiar or new environments. This form of spatial memory is essential for traveling from one place to another (such as from your house to the supermarket) but also for finding your way inside a building (e.g. inside the supermarket). It involves planning the route in advance and continuous updating of your spatial knowledge (these are spatial working memory functions) as the environment will constantly change during a journey. Different strategies can be used for route learning. One strategy is generating a cognitive map of the environment in memory in which the spatial lay-out of the environment is represented in your mind (Bohbot, Iaria & Petrides, 2004; Van Asselen, 2005). This strategy involves spatial learning where one learns the spatial relation between elements (i.e. landmarks) in the environment. As such, you know for example the location of the supermarket in relation to your house or your car. Another strategy is response learning (Iaria, Petrides, Dagher, Pike & Bohbot, 2003; Bohbot et al., 2004; Van Asselen, 2005) in which a route is learned through repetition of rewarded behaviours (e.g. you learn to turn left or right in response to stimuli (e.g. at the post office) as it rewarded you by arriving at the supermarket). Furthermore, the everyday environment can be viewed from different frames of reference: an egocentric or an allocentric frame of reference (Klatzky, 1998). An egocentric (self/viewer-centered) frame of reference is used to code spatial information in relation to the position of the observer whereas an allocentric (other/world-centered) frame of reference is an external reference frame, independent of the viewer’s position. An example of using an egocentric way of coding space is turning ‘left’ or ‘right’ as these directions depend on the orientation of our own body. Another example is when you point in a certain direction (e.g. to show someone else the location of the supermarket), which also depends on your own location as someone else must point in a different direction to appoint the same location. In addition, when pointing towards a certain location, you need to have a spatial layout of the environment in your mind (cognitive map) and to keep this information active until you perform the relevant action (spatial 4 working memory). However, when you use a cognitive map for memorizing a route, you are using an allocentric frame of reference since the relation between two landmarks does not depend on our own position in space. Another distinguished form of spatial memory is object-location memory. This is used for memorizing specific locations for certain objects (Postma & De Haan, 1996; Kessels et al., 2001). Object-location memory is essential in everyday life as you have to remember for example where to find the milk in the supermarket or to recall where you left your car keys. It includes three separate processes: memorizing the identity of an object, memorizing the location of an object, and memorizing the relation between identity and location (Postma et al., 2004). Furthermore, there are two representations to code for the relation between two objects in space: categorical and coordinate spatial relations (Kosslyn, Chabris, Marsolek & Koenig, 1992). When the spatial relation between two objects is specifically encoded in terms of metric distances, one uses coordinate representations. Kosslyn, Koenig, Barrett, Cave, Tang & Gabrielig (1989) proposed that these representations are used to guide actions (e.g. to guide our eyes or arm to move exactly towards an object). Alternatively, when spatial relations are assigned to a category such as ‘above’ or ‘to the left of’, one uses categorical representations. 1.2. Brain areas involved in spatial memory After giving an overview of different components of spatial memory, the question arises whether these forms are functionally and neurologically distinctive or whether they are part of the same system used in different ways. To further explore this issue, the current paragraph presents an overview of evidence for brain structures associated with different forms of spatial memory. The main structures that have been related to spatial memory processes are the hippocampus, prefrontal cortex and posterior parietal cortex (cf. Van Asselen, 2005). The hippocampus has a major role in spatial memory (Burgess, Recce & O’Keefe, 1994) and is involved in many functions of spatial memory (see Burgess, Maguire and O’Keefe, 2002 for a review). First of all, it contains pyramidal cells that are called ‘place cells’ because they are spatially coded (O’Keefe and Dostrovsky, 1971). O’Keefe and Nadel 5 (1978) suggested that these place cells are each restricted to a portion of the environment. The place cells fire when a rat is in a certain location within an environment, independent of its orientation. This indicates that the hippocampus is involved in the processing of spatial information from an allocentric frame of reference (O’Keefe and Dostrovsky, 1971; O’Keefe and Nadel, 1978) and is therefore thought to provide a cognitive map, which is necessary for navigating in space. The concept of a cognitive map for way finding comes from Tolman (1948), who suggested that this cognitive map indicates routes, paths and environmental relationships. An fMRI study, conducted by Hartley, Maguire, Spiers & Burgess (2003), confirmed that the hippocampus “provides a cognitive map” (Hartley et al., 2003 – p. 885) since it showed activation when subjects were accurately navigating via new routes. Second, the hippocampus and the parahippocampal gyrus are associated with object-location memory. That is, the right posterior parahippocampal gyrus has shown activity during recognition of object locations (Johnsrude, Owen, Crane, Milner & Evans, 1999). Furthermore, patients with right parahippocampal or hippocampal lesions have shown deficits in object-location memory (both recall and recognition was impaired) (Bohbot, Kalina, Stepankova, Spackopva, Petrides & Nadel, 1998; Crane and Milner, 2004; Stepankova, Fenton, Pastalkova & Bohbot, 2004). However, Smith and Milner (1989) found impairments in object-location memory in patients with right hippocampal lesions only after a 4 minutes delay. Kessels, Hendriks, Schouten, Van Asselen & Postma (2004) studied patients with amygdala and hippocampal lesions in either the right or the left hemisphere. Patients lacking the left amygdala and hippocampus showed impairments in object-location binding whereas patients lacking the right amygdala and hippocampus showed impairments in coordinate positional memory. Considering the large amount of different results concerning the left or the right hippocampus or parahippocampal gyrus in object-location memory, the specific role of the hippocampus in this component of spatial memory remains unclear. Finally, the hippocampus is essential for encoding spatial information from working memory into long term memory (e.g. Feigenbaum, Polkey & Morris, 1996; Abrahams, Morris, Polkey, Jarosz, Cox, Graves & Pickering, 1999). Feigenbaum et al. (1996) showed that the human right hippocampus is essential for the processing of spatial 6 working memory (which was previously suggested by Olton and Feustle (1981) who studied hippocampal function in rats). In addition, Abrahams et al. (1999) found deficits in spatial working memory as well as spatial reference memory in patients with unilateral atrophy in the right hippocampus. The lateral prefrontal lobe is essential for working memory processes in general such as updating and maintenance of information (Fletcher and Henson, 2001). The dorsal parts of the lateral prefrontal cortex have mainly been related to keeping spatial information active in memory (Nelson, Monk, Lin, Carver, Thomas & Truwit, 2000; Belger, Puce, Krystal, Gore, Goldman-Rakic & McCarthy, 1998; Petrides, Alivisatos, Evans & Meyer, 1993; Jonides et al., 1993). For example, Nelson et al. (2000) studied the functional organization of working memory in 8-11 year old children and found a.o. activation in dorsal aspects of the frontal cortex during a spatial working memory task (whereas ventral aspects showed activations during a non-spatial working memory task). They also found that the activation area was somewhat larger in the right compared to the left prefrontal cortex. These findings were consistent with findings in a study with adults who performed the same spatial working memory task (Casey, Cohen, Craven, Davidson, Irwin, Nelson, Noll, Hu, Lowe, Rosen, Truwit & Turski, 1998). The posterior parietal lobes are engaged in both categorical and coordinate spatial relations (Kosslyn, 1994; Kosslyn et al., 1989). As described above, categorical relations between objects in space are defined by general, abstract codes. Since these categories are language-related, Kosslyn (1994) suggested that the left cerebral hemisphere (dominant for language processing in most right-handed people: Knecht, S., Dräger, B., Deppe, M., Bobe, L., Lohmann, H., Flöel, A., Ringelstein, E.B. & Henningsen, H., 2000) might be specialized in processing categorical spatial relations. He also suggested that the right cerebral hemisphere (associated with navigational processing (Kosslyn et al., 1989)) may be essential for coordinate representations. This lateralization has been confirmed by psychophysical as well as brain imaging studies (see Jager and Postma (2003) for a review). Using visual half field methods, Hellige and Michimata (1989) showed that performance on categorical tasks was better when processed in the left hemisphere and 7 performance on coordinate tasks was better when processed in the right hemisphere. Neuroimaging has also revealed right hemisphere dominance in coordinate tasks and left hemisphere dominance in categorical tasks (Baciu, Koenig, Vernier, Bedoin, Rubin & Segebarth, 1999; Kosslyn, Thompson, Gitelman & Alpert, 1998). All activations were found in parietal areas except for the Kosslyn et al. study (1998), in which left hemispheric dominance for categorical tasks was found in frontal regions. In addition, neural activity in posterior parietal lobes is also associated with navigating through space (route learning) in VR, regardless of the strategy used (cognitive map or response learning) (Aguirre, Detre, Alsop and D’Eposito, 1996; Iaria et al., 2003; Spiers and Maguire, 2006). It has been suggested that these areas together with the anatomically closely linked motor-premotor and supplementary motor areas (Petrides and Pandya, 1984) are involved in higher-level control of movement through space (Milner and Goodale, 1995; cf. Iaria et al., 2003). It has also been reported that medial parietal regions are mainly involved in processing movement through immediate space, whereas lateral parietal regions are mainly involved in planning movement through space beyond instant view (Spiers and Maguire, 2006). Furthermore, the posterior parital cortex has been reported to play a role in egocentric spatial processing (Burgess, Maguire and O’Keefe, 2002) and spatial working memory (Rowe, Toni, Josephs, Frackowiak and Passingham, 2000) which are both spatial memory components that are essential during spatial navigation and route-learning. The caudate nucleus has been related to response learning in rats (Packard, 1999; Packard and McGaugh, 1996). Rats that received a glutamate injection (which stimulates neural activity) in the caudate nucleus predominantly exhibited response learning as a strategy for route learning (navigating), whereas rats that were injected in the hippocampus predominantly exhibited place learning as navigation strategy (Packard, 1999). After blocking hippocampal activity, rats were still able to navigate correctly through a maze, but used response learning instead of place learning as a strategy (Packard and McGaugh, 1996). Using VR, caudate nucleus has also shown activation in humans when participants used response learning as strategy during navigation (Iaria et al., 2003). However, one may question whether this strategy actually is part of spatial 8 memory or not as response learning may in fact be learning an association between a body movement and a stimulus without further spatial information. On the other hand, it can be argued that spatial orientation in relation to the stimulus (a landmark) is necessary in order to make the appropriate body movement. In light of this statement, responselearning can be observed as part of spatial memory as it requires the appropriate spatial knowledge (e.g. determining your own location in relation to a landmark) and the appropriate spatial action (e.g. turning left or right). 2. The organization of everyday spatial memory problems Since spatial memory plays such a major role in everyday life, small failures in spatial memory may have great impact. Most people regularly encounter slight spatial memory failures in everyday life. An example is losing your car keys or forgetting where you parked your car in a large parking lot (object-location memory). Another everyday problem is getting lost in buildings, where people have forgotten how they got to a certain point (route learning) and feel disoriented (cognitive map). Furthermore, some people have problems with converting spatial information from a 2D route map into the 3D real environment (cognitive map, spatial working memory). Other problems concern pointing towards locations that are out of view or giving other people route directions (cognitive map / allocentric representations), estimating distances (coordinate spatial relations) or to recall whether the bakery was above or below the post office in a three store shopping mall (categorical relations). Different types of everyday spatial memory can be distinguished. That is, spatial memory problems can occur over large scale or small scale areas, in short or long term storage, and in a static or dynamic environment. By combining these different types, everyday spatial memory problems can be subdivided into eight different groups: 1. large scale – short term – static 2. large scale – short term – dynamic 3. large scale – long term – static 4. large scale – long term – dynamic 5. small scale – short term – static 9 6. small scale – short term – dynamic 7. small scale – long term – static 8. small scale – long term - dynamic Furthermore, a distinction can be made between prospective and retrospective spatial memory. With this distinction, the spatial memory problems that are organized into these eight different groups could each be either prospective or retrospective. The next paragraphs explain the content of each type of spatial memory problems. Large and small scale Spatial memory can cover small (within one room) as well as relatively large areas (including neighborhoods or even cities and countries). Getting lost on the way from your house to the supermarket, inside buildings or in unfamiliar cities are examples of large scale spatial memory problems. These actions rely on spatial knowledge that covers relatively large areas. We consider space which is larger than can be observed instantly from one single viewpoint as large-scale space (as put forward by Kuipers, 1978). It takes time to gather spatial information about large-scale space by moving through the environment and to put information from multiple viewpoints together to construct a large-scale cognitive map or large-scale route information. Dysfunction in specific forms of spatial memory such as spatial working memory, allocentric spatial ability, or generating a cognitive map may hamper the construction of one single mental layout of space from small pieces of spatial information. This may therefore cause problems with using spatial memory over a large-scale area. Small-scale (or table-top) spatial memory covers information about an area that can be viewed instantly from one single viewpoint such as the spatial layout of the living room or the spatial organization of objects inside a cupboard. Forgetting were you put certain objects can therefore be seen as a small-scale spatial memory problem. Objects in small-scale areas are generally seen as more manipulable (they can be touched and moved) as contrasted with objects in large-scale space (cf. Hegarty, Montello, Richardson, Ishkawa and Lovelace, 2006). This allows people to gather more detailed information about objects in small-scale space. In everyday life, people recall specific 10 locations for specific objects, such as a particular teacup which is located in the left kitchen cupboard and the car keys that are in the second drawer underneath the yellow notebook et cetera. However, problems with processing spatial information from an egocentric frame of reference or object-location memory may cause problems in smallscale spatial environments. An example of integrating small-scale spatial memory with large-scale spatial memory is reading a route-map and subsequently finding your way in the natural environment. This regularly performed action involves converting spatial information from a small-scale 2D map into navigating through a large-scale 3D environment. Some people have problems with map-reading or with converting 2D map information into the 3D natural environment. One might wonder whether this regularly performed spatial action is supported by one system or an integration of two systems for different spatial scales. Hegarty et al. (2006) describe several studies in which it is claimed that both abilities are completely overlapping (the unitary model) or, in contrast, completely dissociated (the total dissociation model). In their own study, they found that small-scale spatial abilities predicted performance on large-scale performance to some extent. Based on these findings they suggested that there should be at least partial overlap between small and large-scale spatial memory. Short and long term Spatial information can be stored in memory for a short period of time (for example in order to be used just once) or for a longer period of time. We label this short term and long term spatial memory respectively. Whether spatial information is stored for short or long periods of time depends on the purpose for which it is needed. If an observer aims to construct a mental layout (cognitive map) while navigating through a new environment, spatial information is aimed to be stored for a long period of time. In addition, when objects are to be stored for longer periods of time, this object-location information should be available for a long period and therefore requires being stored in long term spatial memory. When individuals are unable to process spatial memory from short term into long term memory or when functions such as generating a cognitive map or object- 11 location memory are disrupted, one could encounter problems in using spatial memory for a longer period of time. If you forget which route you just followed in a familiar environment or if you get disoriented fairly easily in new environments, you may have trouble with keeping detailed spatial information active for a short amount of time. Short term spatial memory can specifically be used to remember the exact route you followed during route-learning or navigation. This information may be essential for a short period of time (e.g. in a new environment: to be able to find your way back), but irrelevant to keep in memory for a longer period (when a mental construct of the environment is available and you can find your way back based on a mental layout or when you will not enter the same environment another time). Some object-locations are stored only for a short time in memory: e.g. when objects have a temporary location for instant use (you moved the milk from the fridge to the table only during breakfast). It is irrelevant to store this object-location information for longer periods of time (ordinarily, you can find the milk in the fridge and you do not have to know its specific location on the table during breakfast). Static and dynamic Another distinction which can be made in everyday spatial memory is between static and dynamic use of spatial memory. We consider spatial memory as static when spatial information content is fixed and when it does not involve environmental changes, sequential information or updating of spatial knowledge. A static view of environmental space is associated with mainly an allocentric survey-based ‘from above’ perspective (cf. Postma et al., 2004). An example of problems with static spatial memory is the inability to recall where you left your car keys. It involves finding a stationary object in a fixed environment. To know the relative distance between your house and the supermarket is another example of static spatial memory in the natural environment. Hence, static spatial memory includes object-location memory, knowledge about spatial distances, and knowledge about the spatial lay-out of environments (either small or large-scale). Spatial memory is considered dynamic when it employs changes in the environment, sequential spatial information, planning and updating of spatial information. Postma et al. (2004) put forward that dynamic spatial memory often engages 12 a ‘from within the environment’ perspective (which mainly involves egocentric representations of space). Getting lost when you travel from one place to another (which constantly requires locating yourself in the environment, updating spatial knowledge about the changing environment, and planning the route ahead) is an example of problems with dynamic spatial situations. It involves sequences of different spatial environments as well as sequences of spatial decisions. Another everyday example is giving someone else route directions in which you have to mentally walk through the environment. This involves similar dynamic use of spatial memory as when you are traveling through the environment yourself. Problems with spatial working memory, response learning or route-learning may therefore disrupt the dynamic use of spatial memory (or the use of spatial memory in dynamic situations). Prospective and retrospective Spatial memory can be used to look forward in time (prospective) or to recall previous spatial information (retrospective). Prospective spatial memory involves planning in advance and having expectations about future spatial situations. When you are traveling from one place to another or navigating through a building, you plan the route in advance in order to know when to turn left and right before arriving at your destination. You have an expectation about the consequences of each action: e.g. when you turn left at the post office you expect to get closer to the supermarket. When navigating through a new environment you also plan to take the best route and have expectations about future spatial situations although you do not have an exact mental image of the spatial layout. In a new building for example, when you climb the stairs you may expect that the next floor will have a similar floor plan as the former one and thus you expect to be able to go left when you get upstairs. Several studies have examined route-planning behaviour in humans (e.g. Elliott, Frith and Dolan, 1997; Maguire, Frackowiak and Frith, 1996; Spiers and Maguire, 2006). Spiers and Maguire (2006) for example studied route-planning behaviour of taxi drivers in a highly accurate computer simulation of a real-world environment (the city of London, UK). Using fRMI they reported several brain areas (a.o. the hippocampus, retrosplenial cortex and posterior parietal cortex) that were activated specifically during route-planning. Another example of using prospective spatial memory 13 is when you are planning where to store certain objects (e.g. you plan where you are going to leave your car keys in order not to lose them next time). In addition, when you move objects to make room for others you have to predict how much space will be available when you remove something. This involves a prospective view of the spatial layout of the environment. We suggest that prospective spatial memory mainly requires spatial working memory (planning) but also the ability to generate allocentric cognitive maps about the spatial layout since you have to make predictions about a spatial environment beyond the current view. Retrospective spatial memory involves the ability to recall previous spatial information. This involves keeping track of where you are in a new environment (of which you have not constructed a cognitive map yet), of where you left certain objects in space, or to recall the spatial layout of the parking space (in order to find your car back). Retrospective spatial memory is used to remember the spatial layout of where you have been or the route that you have followed (whilst planning where to go next). Studies in which subjects are required to retrace a previously traveled route (e.g. Cherrier, Matsumoto, Amory, Asthana, Bremner, Peskind, Raskind and Craft, 2005; Van Asselen, Fritschy and Postma, 2006) or in which subjects are asked to recall object-locations (e.g. De Goede and Postma, 2008; Postma, Kessels and Van Asselen, 2008 (review)) are examples of measuring retrospective spatial memory. Everyday problems in retrospective spatial memory occur when people forget where they left certain objects or how they got to a certain location. An evident example of relying on retrospective spatial memory is when you have lost something during a journey from one place to another and you have to follow the exact same route back. To conclude this chapter, everyday spatial memory problems can be organized into eight different groups. A spatial memory problem is assigned to a certain group based on whether the problem involves either large or small scale areas, short or long term storage and static or dynamic environments. ‘Forgetting where you left your car keys’ for example could be assigned to group 5 (small scale – short term – static) or group 7 (small scale – short term – static) depending on how long the keys where in a certain location. This problem would also be a retrospective spatial memory problem as it involves the 14 ability to recall previous spatial information. Problems with giving route directions or with planning a route in a familiar environment would fit into group 4 (large scale – long term – dynamic) as it covers large scale spatial information that is stored in long term memory involving changes in the environment and sequences of actions. Furthermore, this problem is a prospective memory problem as it involves planning and expectations about future spatial environments. 3. Underlying factors of everyday spatial memory problems Most people encounter problems with several aspects of spatial memory to a small extent in everyday life. However, some people encounter spatial memory problems to a larger extent than others. To answer the question why some people have more spatial memory problems than others, several neurological and psychological factors that may cause problems with everyday spatial memory are summed up in this chapter. 3.1. Age It is generally known that memory weakens with age. These impairments mainly involve spatial problems as one of the first things that elderly people complain about is losing the ability to navigate in new environments (Burns, 1999). As a result, elderly people start to avoid unfamiliar routes and places. Animal studies have confirmed that spatial memory grows weaker with age (see Barnes, 1988 for a review). These age-related deficits in spatial tasks (such as place learning or route learning) have mainly been associated with hippocampal changes: such as increased decay in long-term potentiations (Bach, Barad, Son, Zhuo, Lu, Shih, Mansuy, Hawkins and Kandel, 1999; Barnes and McNaughton, 1987) and a decrease in accuracy of information processing of older hippocampal neurons (Barnes, Rao and McNaughton, 1987; Barnes, 1988). In humans, aging is in general associated with memory impairments. A common characteristic of age-related diseases as for instance Alzheimer’s, is that elderly people get lost even in familiar environments. However, also normal aging (i.e. excluding age-related diseases) has been associated with increased impairments on all spatial memory components. A variety of studies illustrate that older healthy adults perform poorer than young adults on tasks that require spatial working 15 memory (e.g. Salthouse, Babcock and Shaw, 1991), route learning (e.g. Kirasic and Mathes, 1990; Kirasic, 1991; Kirasic, Allen and Haggerty, 1992; Wilkniss, Jones, Korol, Gold and Manning, 1997; Moffat, Zonderman and Resnick, 2001), and object-location memory (e.g. Cherry and Park, 1993; Schiavetto, Köhler, Grady, Winocur & Moscovitch, 2002). Memory impairments associated with aging mainly involve allocentric spatial memory: remembering spatial relationships between landmarks and objects in large environments as well as learning a route from a map is impaired with age (cf. Rosenzweig and Barnes, 2003; Moffat, Elkins and Resnick, 2006). Moffat and Resnick (2001) for instance, studied the effects of aging on navigation and the use of a cognitive map using virtual reality (VR). They demonstrated that the performance of old adults on this route learning task was impaired compared to young adults. In a follow-up study, they demonstrated that normal aging is associated with traveling longer distances to locate the goal, spending less time to navigate the environment and impairments in constructing a cognitive map (Moffat and Resnick, 2002). Many age-related changes in a healthy human brain are initially observed in the hippocampal area (Tomlinson and Henderson, 1976; Lupien, Leon, Santi, Convit, Tarshish, Nair, Thakur, McEwen, Hauger and Meaney, 1998; Grady, McIntosh and Craik, 2003; Maguire and Frith, 2003). This is in line with age-related memory problems. Since the hippocampus is involved in the majority of spatial memory components, the hippocampal age-related changes may explain the variety of spatial memory problems in elderly people. Furthermore, neuroimaging has revealed that during spatial navigation, elderly people show reduced activity in the hippocampus and parahippocampal gyrus, but increased activity in anterior cingulate gyrus and medial frontal lobe in comparison to younger people (Moffat et al., 2006). Increased activity in these frontal areas may indicate that older adults show compensatory shifts in neural activity or that the navigation task was more demanding for aged people. Moreover, several other studies found functional as well as structural changes within the prefrontal cortex (ReuterLorenz, Jonides, Smith, Hartley, Miller, Marshuetz and Koeppe, 2000; Tisserand and Jolles, 2003), which may be related to either a compensatory shift in neural activity (i.e. the same memory system taken over by different brain areas) or with the use of different strategies to encode space. 16 3.2. Gender Research on human sex differences in spatial memory is increasing (Postma et al., 2004). In contrast to the general agreement that men are superior on spatial memory, there is no such thing as one unitary superior spatial memory system. As described in chapter one, spatial memory consists of multiple components which are together as well as independently essential for multiple everyday activities. The question is: to what extent do men outperform women or do women outperform men with regard to spatial memory? And which everyday memory problems could be attributed to sex-differences? Several studies, using the Corsi Block-Tapping task, demonstrated that men have a larger spatial working memory span compared to women (Orsini, Chiacchio, Chinque, Cocchiaro, Schiappa and Grossi, 1986; Capitani, Laiacona and Ciceri, 1991). In contrast, a study by Postma et al. (2004) revealed no sex differences while using the same task, but a smaller number of subjects. This indicates that the sex-differences on spatial working memory may be relatively small. On a route learning experiment, men outperformed women on learning a route on a map and on remembering metric properties, whereas women were able to recall more of the landmarks (Galea and Kimura, 1993). This may indicate that women may use different strategies to move around in everyday life (such as relying on specific landmarks) than men (generating a cognitive map of environmental layout whilst ignoring environmental details/landmarks). A study by De Goede, Berthoz, Zaoui and Postma (submitted) showed that this difference in strategy was not the result of inabilities in processing geometric cues in women, as men and women performed equally on pointing towards a start position in the absence of visual landmarks during encoding as well as retrieval. In a virtual environment, men were faster than women at finding their way out of a complex, three-dimensional maze (Grön, Wunderlich, Spitzer, Tomczak and Riepe, 2000). However, studies in natural environments revealed no such differences (Worsley, Recce, Spiers, Marley, Polkey & Morris, 2001; Lewin, Wolgers & Herlitz, 2001; Lawton & Charleston, 1996) except for Silverman, Choi, Mackewn, Fisher, Moro & Olshansky (2000) who found an advantage for men to navigate through a wooded area. This indicates that in most natural environments, women do not encounter more problems with route finding than men. Furthermore, women have shown superiority in several 17 object-location tasks: i.e. recognizing objects that have exchanged position (Eals and Silverman, 1994; James and Kimura, 1997) and the legendary game Memory (McBurney, Gaulin, Devineni and Adams, 1997). This superiority was confirmed by a recent metastudy (Voyer, Postma, Brake and Imperato-McGinley, 2007). In contrast, men have shown superiority in object-location memory for nonsense objects (inkblots) (Lewin et al., 2001) as well as identical objects (Postma, Izendoorn and De Haan, 1998). This indicates that men outperform women on positional memory (without object identification). These findings are consistent with findings on spatial memory tasks that require coordinate coding of space such as an advantage for men in estimating distances (Postma et al., 2004). In a recent study by De Goede and Postma (2008), women appeared to outperform men in overall object location memory, whereas similar performance for men and women was found on isolated object identity memory and object-location binding. Postma, Winkel, Tuiten and Van Honk (1999) revealed that sex-related differences in spatial memory may be influenced by sex hormones as females performed better in the nonmenstrual phase compared to during menstruation. fMRI has revealed different patterns of activation for men and women during a virtual maze task: distinct activation in the left hippocampus in males and increased right parietal and right prefrontal activity in females (Grön et al., 2000). In a different fMRI study using a spatial task (judgment of line orientation) showed bilateral activation in lateral frontal and midtemporal regions in men whereas this activation was restricted to the right hemisphere in women (Gur, Alsop, Glahn, Petty, Swanson, Maldjian, Turetsky, Detre, Gee & Gur, 2000). This suggests that differences in lateralization may underlie sex differences on spatial memory performance. 3.3. Neurological damage As described in chapter 1.2., focal lesions can impair spatial memory abilities. Specific lesions in specific brain areas cause problems in particular spatial memory components and therefore in particular everyday spatial actions. Lesions in the hippocampus for example have been associated with impairments in object-location memory (Smith and Milner, 1989), object-location binding and coordinate positional memory (Kessels et al., 18 2004), and spatial working memory (Abrahams et al., 1999). These specific lesions should therefore mainly disrupt everyday spatial abilities in a static environment or in an environment that requires a static mental representation of space such as relocating car keys or the car in a parking lot, or judging the exact location of objects in space, and reaching and grasping for these objects. Lesion in the hippocampus may cause impairments in small scale areas, but will certainly impair large scale mental representations as the hippocampus is essential for building a cognitive map (Hartley et al., 2003). Lesions in dorsolateral prefrontal cortex are found to impair spatial working memory (e.g. Bechara, Damasio, Tramel and Anderson, 1998) and may therefore impair behaviour in dynamic environments (or in environments that require dynamic spatial representations) and behaviour in environments that require prospective spatial memory (which involves a.o. planning of future spatial actions and situations). Neurodegenerative disorders such as Alzheimer’s dementia and Parkinson’s disease are related to neuronal loss in a variety of areas (Panegyres, 2004). Alzheimer’s disease is the commonest form of neurodegenerative disorders and has mainly been associated with spatial memory deficits (De Tolledo-Morrell, Dickerson, Sullivan, Spanovic, Wilson and Bennett, 2000; Kohler, Black, Sinden, Szekely Kidron, Parker, Foster, Moscovitch, Wincour, Szalai and Bronskill, 1998), which are correlated with Alzheimer related hippocampal atrophy. Alzheimer’s patients will therefore encounter most problems with getting lost due to impairments in generating or using a cognitive map. These patients will even get lost in familiar environments. Parkinson’s disease may be associated with deficits in spatial working memory and memory for object locations as a result of neuronal atrophy in prefrontal cortex, dopaminergic pathways and striatalfrontal circuits (cf. Panegyres, 2004). Parkinson’s disease patients may therefore encounter more problems with losing objects and with the majority of everyday activities that require spatial working memory such as traveling (which causes the environment to change and which therefore demands the ability to update spatial information). 3.4. Visual impairments Visual impairments alter behaviour in the natural environment and influence the development and use of spatial memory. The main visual impairment associated with 19 spatial memory problems is total blindness, but other visual impairments such as lowvision or monocular vision may also affect everyday spatial memory. In sighted people, the generation of spatial representations through auditory experience still requires the visual system (Zwiers, Van Opstal and Cruysberg, 2001) and tactile stimuli are typically remapped in coordinates that are modulated by vision (Hötting, Rösler and Röder, 2004). These studies demonstrate that vision is the primary sensory modality of spatial cognition (see also: Eimer, 2004) and the loss of vision should have major impact on everyday spatial memory (for a review on impaired spatial cognition in visually impaired individuals see: Cattaneo, Vecchi, Cornoldi, Mammarella, Bonino, Ricciardi and Pietrini, 2008). Research has shown that early blind people have specific problems with spatial processes that require active integration and transformation, whereas passive storage of spatial information is similar to sighted people (Cornoldi and Vecchi, 2000). Pasqualotto and Newell (2007) found that the updating of a haptically learned spatial environment is impaired in blind people. Noordzij, Zuidhoek and Postma (2006) demonstrated that blind individuals generate a route-based representation of the environment instead of a surveybased cognitive map in sighted people. This finding implicates that blindness can make moving through the environment less flexible (when a route is blocked, it would be difficult to find an alternative route without knowledge of the spatial layout). This finding also implicates that blind people mainly rely on egocentric response learning and that their spatial memory largely contains dynamic spatial information. In addition, blind people perform poorly on other survey based spatial tasks such as estimating Euclidean distances between locations (Rieser, Lockman and Pick, 1980) and pointing towards locations in a room (Rieser, Guth and Hill, 1986). However, studies using tactile maps indicate that survey-based representations do exist in blind individuals (Espinosa, Ungar, Ochaita, Blades and Spencer, 1998) and that blind people can even outperform sighted people on survey-based tasks (Tinti, Adenzato, Tamietto and Cornoldi, 2006). This signifies that blind individuals are very well able to convert small-scale spatial information on a map into large-scale 3D natural environmental space. One can imagine that visually impaired people who suffer from severely reduced visual capacity and require external devices to manage everyday activities may also be impaired on spatial memory. However, visually impaired children and adults performed 20 better than blind children and adults on a variety of spatial tasks (Bigelow, 1996; Blanco and Travieso, 2003; Byrne and Salter, 1983). Moreover, their performance was similarly to sighted people (Bigelow, 1996; Blanco and Travieso, 2003; Vecchi, Cattaneo, Monegato, Pece, Cornoldi and Pietrini, 2006). Only one study by Passini, Proulx and Rainville (1990) showed that visually impaired individuals may show selective impairments on route inverting, choosing shortcuts and mental rotations due to the inability to use distant cues and visual reference points. Overall, findings on visually impaired individuals suggest that the brain can use poor quality visual information to generate adequate cognitive maps with appropriate visual layouts in spatial memory Monocular vision is associated with reduced perception of depth as a result of absent stereoscopic vision (Von Noorden, 1996). This affects a.o. depth judgments, reaching, balance and orientation (Howard, 2002). These inabilities may also influence spatial memory. Vecchi et al (2006) showed that monocular individuals were to a similar extent as blind individuals impaired on an object-location memory task that required imagery. Further research should clarify to what extent monocular vision may affect specific everyday spatial memory abilities. 3.5. Stress and anxiety Another factor that is known to influence spatial memory is stress or anxiety. Research on animals revealed that chronic exposure to stress leads to decreased dendrites, decreased length of dendrites, and cell loss in the hippocampus (Watanabe, Gould and McEwen, 1992; Woolley, Gould and McEwen, 1990; Uno, Tarara, Else, Suleman and Sapolsky, 1989). Luine, Villegas, Martinez and McEwen (1994) demonstrated that chronic stress also leads impairments in hippocampal function: spatial memory performance was reversibly weakened. Diamond, Fleshner, Ingersoll and Rose (1996) showed that psychological stress impairs spatial working memory as rats exposed to stress performed poorly in novel environments. In humans however, research on stress has not shown obvious impairments in spatial memory. Schwabe, Oitzl, Philippsen, Richter, Bohringer, Wippich and Schachinger (2007) studied the influence of stress on spatial learning and discovered that psychosocial stress prior to learning reduces the use of spatial learning strategies: stressed participants switched to stimulus-response 21 strategies more often than controls. This implicates that stressed individuals favor the use of caudate nucleus-dependent strategies over strategies that require the hippocampus (which is in line with animal studies that show stress-induced impairments of hippocampal function). Whether this stress-related change in spatial learning strategy is the result of decreased hippocampal function is not clear. A recent study revealed that chronic stress (in addition to acute stress) increased the use of stimulus-response strategies instead of spatial strategies in mice as well as humans (Schwabe, Dalm, Schächinger and Oitzl, 2008). In a study carried out by Lawton (1994) an indirect relationship was found between spatial ability and spatial anxiety: the use of an orientation strategy (maintaining a sense of your own position relative to environmental landmarks) instead of a route strategy was positively correlated with spatial perception and negatively correlated with spatial anxiety. Furthermore, Schmitz (1997) found gender differences in spatial memory performance which could be explained to a certain extent by different levels of anxiety and fear: girls (who scored higher on anxiety and fear scales than boys) moved more slowly through a maze, recalled more landmarks and fewer directions than boys. Furthermore, all subjects (i.e. boys and girls) who scored high on fear and anxiety showed similar results, although not completely significant. Hence, stress and anxiety could impair spatial ability to a certain extent. In humans, the influence of stress on behaviour in space is mainly expressed in the use of non-spatial strategies which implicates specific impairments or at least cognitive restrictions on spatial memory. 3.6. Mood A small amount of studies have focused on the influence of mood on spatial memory. However, if emotional state affects spatial memory performance, one can imagine that if navigation or route finding in emergency situations is impaired, the consequences may be catastrophic. Miller, Fujioka, Chapman and Chapman (1995) revealed that spatial performance on a positional task (remembering the positions of dots in a display) was impaired in participants with major depression. In addition, Tucker, Hartry-Speiser, McDougal, Luu and deGrandpre (1999) found that subjects high in negative arousal did not show a right hemisphere advantage for spatial processing (using visual half-field 22 methods) which was present in subjects with normal arousal levels and which is in line with a right hemisphere dominance for spatial attention (Corbetta, Miezin, Shulman and Petersen, 1993). Subjects with high negative arousal levels also showed an altered pattern in EEG response to spatial stimuli. This indicates that emotional state may alter spatial memory or the use of spatial memory. Brunyé, Mahoney, Augustyn and Taylor (in press) are the first to report that high arousal states, either positive or negative, amplify the symbolic distance effect (Moyer, 1973) in which the distance between two landmarks that are relatively far away from each other are judged with faster response times and higher accuracy compared to the distance between two landmarks that are relatively close together. Subjects that studied a map in high arousal states performed better on judging global spatial relations relative to controls, which indicates that high arousal may improve the development and subsequent use of spatial memory. Subjects that studied the map in low arousal states performed poorly on distal comparisons relative to both controls and subjects inv high arousal states. Furthermore, low arousal levels did not improve judgments about the distance between proximal landmarks which indicates that low arousal may impair either spatial attention or spatial memory or both (Brunyé et al., in press). To summarize, in the above chapter we have reviewed a large amount of literature demonstrating that several factors such as age, gender, lesions, blindness and even psychological factors such as stress, anxiety and mood may alter spatial memory and may cause specific problems in the use of spatial memory in everyday life. To measure exactly which problems occur in everyday life and to what extent specific impairments cause everyday problems, future research should focus more on spatial memory impairments caused by factors described above in ecological settings (i.e. natural or close to natural environments). 23 4. Measuring spatial memory in everyday life As moving through the everyday environment or recalling spatial information about your natural surroundings involves combined functioning of numerous components of spatial memory, one might wonder whether laboratory studies measure spatial memory as it is used in everyday life. In laboratory research, specific components of spatial memory can be studied in isolation whereas in everyday life, spatial memory will always be applied in a multidimensional way, using different components of spatial memory combined to get the most effective results. Furthermore, the natural environment is usually much more complex than laboratory spatial situations by, for instance, providing much more stimuli (visual as well as auditory and vestibulo-tactile) which can either facilitate or impede the use of spatial memory. To explore spatial memory in everyday life, one could study people’s personal experiences with spatial memory problems, specific forms of spatial memory in experimentally controlled virtual environments, or specific forms of spatial memory in ecologically valid natural environments. In this chapter, an overview is presented of these three measures and how each measure might contribute to knowledge about everyday spatial memory use and problems. Furthermore, the construct validity, external validity and internal validity of each measure is discussed. 4.1. Survey research / questionnaires Surveys or questionnaires are a suitable method to obtain a large amount of data from a large number of people. It is a structured set of questions to gather information from a group of people about their experiences, beliefs, values or tendencies to act. It could give an overview of problems that are experienced in everyday life and how spatial memory is applied in the natural environment. Surveys could also measure which strategies are used in different environments or situations, how frequently specific problems occur in everyday life, or how people cope with these spatial memory problems. Questionnaires on spatial memory are regularly used to measure the extent to which dementia or Alzheimer patients encounter problems in the everyday spatial environment with the aim to enhance the development of effective interventions, of adequate residential environments or to improve their wayfinding efficiency (c.f. Chiu, Algase, Liang, Liu & Lin, 2005; Wilson, Cockburn, Baddeley and Hiorns, 1989). Other examples of 24 questionnaires that measure everyday memory performance are the Inventory of Everyday Memory Experiences by Hermann and Neisser (1978), the Cognitive Failures Questionnaire by Broadbent, Cooper, Fitzgerald and Parkes (1982), and the Head Injury Postal Questionnaire by Sunderland, Harris and Gleave (1984). Construct validity: Construct validity concerns the adequacy of the independent and dependent variables in a study. In a questionnaire one may question whether different items are the best ones to measure specific forms of spatial memory. One may also question whether questions are the best method to measure how everyday spatial memory is used in everyday life. However, questions are the best way to measure someone’s personal experience with everyday spatial memory problems. It could also contain many items which results in a fairly broad view on these problems and may therefore include problems that may not occur during specific experimental tasks. Internal validity: The major problem with memory questionnaires is that responding to items in itself is a memory task and that they are based on the participant’s metamemory (which would most certainly become a problem for patients with memory impairments). Will a person’s subjective report give an objective image of spatial memory performances (e.g. do some spatial memory problems have more impact on a person’s life and may therefore be rated as occurring more frequently than in reality)? Questionnaires may thus be susceptible to biases such as responding as subjects feel they should instead of what they truly believe or judging the frequency of certain problems wrongly as a result of the impact of a certain spatial problem. Another problem with questionnaires is that subjects may give incorrect responses as they cannot accurately judge their spatial memory abilities (Herrmann, Grubs, Sigmundi and Grueneich, 1986). However, questionnaires can be constructed to avoid these problems. An example is using closed and very specific questions instead of open questions. If explicit examples are used and specific answers are required (e.g. on frequency questions explicit numbers per day, week or month can be enforced), a person can be guided towards the most realistic answers. Furthermore, multiple items can be used that measure the same aspect. Whether these questions actually measure the same aspect can be tested by means of factor analysis as carried out for example by Chiu et al. (2005) on a newly developed 25 Everyday Spatial Questionnaire for Dementia patients or by Wilson et al. (1989) to test the validity of the Rivermead Behavioural Memory Test. External validity: As questionnaires can be completed by a broad range of people and questions are fairly unlimited, the findings can quite easily be generalized to larger populations and different environments. The only problem that might occur in ecological validity (i.e. the relevance for everyday cognition and activities) is that participants may be biased and their answers may not equal their everyday spatial actions. This problem arises because questionnaires do not measure behaviour directly, but they measure how people judge their own spatial behaviour. However, as described above, questionnaires can be constructed to avoid these problems. Hence, the construct and external validity of surveys are quite good, but the internal validity may be at risk. Items that are well constructed (which are appropriate, detailed and clear) may enhance the internal validity. Furthermore, data from questionnaires with closed questions are well quantifiable: items that are rated on a scale provide numbers as data which are easily used for analyses. 4.2. Virtual Environments An increasing amount of studies use 3D virtual environments (VE) to investigate human spatial memory in everyday environments. Virtual reality can be used to create a realistic simulation of the natural everyday environment in which a person can navigate, follow routes, move back and forth, and make 360 degree turns. Hence in a VE, a person can perform similar spatial behaviour as in the real-world environment. A VE can resemble the interior of a building, streets in a city or some other outside environment with as many landmarks, road obstructions or other objects and situations that can be encountered in the real world. Along with trainings for various occupations such as drivers (Mahoney, 1997), pilots (Lintern, Roscoe, koonce and Segal, 1990), and soldiers (Goldberg, 1994; Goldberg, and Knerr, 1997), VEs are used to assess spatial abilities of patients with cognitive impairments for rehabilitations purposes (Brooks and Rose, 2003) or to study spatial memory in general (Hurlebaus, Basten, Mallot and Wiener, 2008; Maguire, Burgess and O’Keefe, 1999; Maguire, Spiers, Good, Hartley, Frackowiak and 26 Burgess, 2003). Hurlebaus et al. (2008) for instance, studied route learning strategies in a complex and cluttered VE. The VE lacked unique landmarks or road networks, and the only distal cues were four large coloured columns. They discovered strong differences in route learning strategies between individuals with some participants being conservative and others showing high variability in their route choices. The conservative participants could reproduce the route without local landmarks and thus relied on metric information whereas participants who showed high variety in route choices strongly relied on the global landmarks. Construct validity: The construct validity in VEs can be very good. To measure for example route learning in an unfamiliar environment, this VE can be created and participants can navigate in a similar way as in real life. Hence, the appropriate environment can be constructed to measure the appropriate form of spatial memory or everyday problem. Internal validity: The main advantage of a VE is that the environment, as contrasted with the real-world environment, is completely controlled. This means that confounding variables are reduced to a minimum. Furthermore, the VE can be a simulation of an existing environment, but it could also be a newly invented environment which would eliminate familiarity as potential confounding variable as well. Another advantage of VEs is the ability to use fMRI to study neural activation during navigation and route-learning (which normally requires movement) (e.g. Maguire, Burgess and O’Keefe, 1999). External validity: Although VEs are designed to be as close to natural as possible, several limitations can be pointed out. First of all, the field of view is limited to the size of a monitor and therefore typically narrower than the field of view available in the real world. Second, the screen will always have reduced resolution which makes a virtual environment look different from a real environment. A third and most important limitation of VE research is that moving through a PC-based virtual environment does not require actual movement. Navigation is thus based on merely visual information in the absence vestibular and proprioceptive information. For these reasons, one could question whether findings in VEs could be generalized to real-world environments. Some studies have shown that this form of generalization is possible. Ruddle, Payne and Jones 27 (1997) for instance, have demonstrated that spatial memory performance in VEs and in real world environments are comparable. They found that people learn to navigate inside VEs with accuracy similar to inside real buildings. Their study also demonstrated that making VEs more realistic with everyday objects for landmarks as an alternative of using cubes with abstract patterns, improved navigation performance. Furthermore, Munzer and Stahl (2008) observed that an animated virtual walk instruction significantly improved performance during the actual walk in a real building compared to route instructions in the form of an allocentric map or egocentric sequences of pictures. In contrast, Skorupka (2008) and Ruddle and Jones (2001) reported that the navigation pattern in VEs differs from navigation patterns in real environments: in VEs, as contrasted with real world environments, people tend to follow generally straight paths. As a result, the time to reach a destination (an elevator) was longer in a virtual building than in a real building (Skorupka, 2008). Furthermore, a study by Farrell, Arnold, Pettifer, Adams, Graham and MacManamon (2003) reported that VE training did not provide better route learning than studying a map. They also demonstrated that VE training in combination with studying a map did not improve performance compared to studying a map alone. This indicates that VEs may not transfer well to the real world. As made obvious by the foregoing, spatial behaviour in VEs and real environments is not necessarily equivalent. Therefore, to study spatial memory in a VE may not be as accurate as in a real-world environment. This is possibly due to the limitations described earlier. However, as technologies are developing, more naturalistic VEs can be generated. Bulthoff, Campos and Meilinger (2008) describe VEs in which the field of view can be larger and displays can have high resolutions. Furthermore, sophisticated self-motion interfaces have been developed where participants can navigate inside VEs through actual walking. Bulthoff et al. (2008) also notify that limited walking is made possible by omni-directional treadmills. One major disadvantage of these advanced VEs is that they are far more expensive than the use of PC-based VEs. 4.3. Spatial tasks in natural environments When you measure spatial memory in everyday environments, two decisions must be made: 1) which environment should be selected and 2) which task will measure the aspect 28 you want to measure. To explore different aspects of everyday spatial memory, a variety of spatial tasks can be carried out in natural settings. Before we discuss the validity of measuring in natural settings, we present an overview of different methods to measure spatial memory in natural environments. Pointing When you point towards certain objects in space that is out of view, you have to first determine your own position in the environment, subsequently the position of the object in space, than you orient towards the object in space and finally you move your hand in the appropriate direction. Lemay and Proteau have implemented several studies in which they used manual pointing as a measure for effects of aging (2002, 2003), visual background information (Lemay, Gagnon and Proteau, 2004), and movement duration (2001). Among others, these studies show that pointing towards unseen targets can be used to assess how target location can be specified in an egocentric frame of reference that are encoded in either an egocentric or an allocentric frame of reference. Moreover, pointing has also been used to assess configurational knowledge about the spatial layout of the environment (De Goede, Berthoz, Zaoui and Postma, submitted; Rieser, Guth and Hill, 1986). None of these studies however, were carried out in a natural environment: in the Lemay and Proteau studies, participants were pointing towards a computer screen and De Goede et al. used a virtual environment. We suggest that pointing towards target locations could also be measured in the natural environment in order to measure e.g. large-scale object-location memory from an egocentric perspective or how well metric aspects of the environment are processed in an ecologically valid setting. Furthermore, different natural settings may show how different contexts (i.e. different environments) may help or impair pointing abilities. Pointing accuracy can be quantified by measuring the absolute angular error in degrees (cf. Mou, McNamara, Valiquette and Rump, 2004). On condition that a scaled map is available, the accuracy in angular degrees can be assessed in every possible environment. 29 Way finding Another method to measure spatial memory in real-world environments is to let people navigate in actual buildings or cities. This method has been used in several studies in the natural environment (e.g. Chang and Fotios, 2008; Munzer and Stahl, 2008; Van Asselen et al., 2006). In the study by Van Asselen et al. (2006), incidental learning was compared to intentional learning during a walk through a building. Chang and Fotios (2008) explored way finding behaviour in unfamiliar buildings in order to investigate whether buildings could be designed to improve way finding. Objective information can be gathered during route learning or way finding in real environments: Van Asselen et al. for example scored recalled landmarks in the correct position and order, number of correct decisions on a map drawing task and during route reversal navigation, and finally had the distance estimated in meters. Chang and Fotios also used decision points to analyze the routes and looked at how often certain strategies were used (calculating the percentage following a certain strategy on all decisions). These examples indicate that way finding behaviour in real environment can be studied and quantitative data can be obtained. Verbal route instructions Another interesting issue in everyday spatial memory concerns how well humans can verbally describe routes (e.g. from the post-office to the supermarket). It could be a measure of allocentric spatial memory: how well do people know spatial relations between landmarks (i.e. between the post-office and the supermarket, or between the post-office and the church where you have to turn left)? Furthermore, it could be observed how much details a large-scale cognitive map may encompass (in terms of either landmarks or metric distances and configurations). In a study to further develop human-robot communication, it is observed that a robot can transform human verbal route instructions into a metrical route graph (Bauer and Buss, 2008). This demonstrates that verbal route instructions can be transformed into quantitative data and utilized to assess the accuracy of these instructions. We consider therefore that verbal route instructions in the natural environment could give a proper representation of the cognitive map that people generate and use of this map in everyday life. 30 Locating oneself on a map To locate yourself on a map you require the ability to orient yourself in the environment, convert 3D spatial information into 2D from above view and estimate the spatial relations between yourself and surrounding objects (e.g. buildings or roads). To explore how well people can orient themselves in a familiar or unfamiliar environment, or to what extent people can generate a ‘from above’ view of the environment one could have people locating themselves or other objects on a map. For instance, Liben, Myers and Kastens (2008) studied people’s abilities to mark their locations on a map and found that performance varied widely across individuals. Performance on a specific spatial task (i.e. a paper folding task assessing spatial visualization) predicted performance on the mapping task. This method is a suitable measure to assess a person’s ability to convert natural environmental large scale space into small scale 2D from above view. Again, objective and quantitative data can be obtained which makes it a useful method to compare different groups or spatial abilities in different situations. Large-scale object locations To measure the use of spatial memory in a relatively large-scale and static natural environment, one could have people recall the locations of certain objects in an everyday environment. Lutz, Means and Long (1994) carried out a study on a large parking lot. They measured everyday object-location memory by letting people recall where they parked their car. Several tasks were performed in this study: participants marked the location on a map (measuring allocentric cognitive map abilities) and reported which strategies they used for remembering the location (or for getting back to the car). A similar experiment was carried out by Plukaard, Van Oers, Back and Postma (unpublished), using an even larger parking lot and more participants. Along with defining strategies used and marking the location of the car on a map, the distance between a predetermined location and the location of the car was estimated (to test coordinate coding of space), and a pointing task was performed (to test egocentric abilities, participants were asked to point towards the location of the car). These studies show that many different aspects of spatial memory can be assessed and that objectlocation memory in a large-scale everyday environment may involve many components 31 of spatial memory. The individual tasks to measure large-scale object location behaviour can give quantitative results. By selecting the appropriate environment (in the latter study: a parking lot in front of a shop) and by obtaining information about the familiarity of the environment, current mood and other personal issues that may affect spatial memory performance, confounding variables can be reduced to a minimum. Construct validity: As many different tasks can be carried out in everyday settings and as the use of spatial memory is measured in settings in which it is actually used, these tasks are the best way to measure everyday spatial memory. Nevertheless, one should always make sure that the appropriate task is chosen to measure a certain form of spatial memory. That is, ‘pointing’ should be used to measure orienting, allocentric cognitive map abilities and not to measure dynamic spatial memory abilities such as navigation. Internal validity: One disadvantage of measuring in the real environment is the increased probability of confounding variables that may lead to unreliable results. For instance, specific sounds can be used (and are used in everyday life) as spatial cues: an experimental session in which a church bell rings may lead to different results than a session in the same environment in the absence of this sound. Therefore, the experimenter should seek to minimize confounding variables such as specific sounds or other external cues, familiarity of the environment (which should be similar to all participants), and weather conditions (rain or fog can change the appearance of the environment). However, complete elimination of confounding factors is almost impossible in field research. Another problem with measuring in the real-world environment is that it is difficult to repeat a study in a real environment as environments change through time. This is also the advantage of measuring spatial memory in everyday environments since spatial memory is normally applied in changeable settings. To find similar results in repeated studies in a changing environment will therefore strengthen spatial memory findings. External validity: The major advantage of measuring in the real environment as an alternative of measuring in laboratory settings is that you can measure the behaviour as it most likely would be in everyday life. In laboratory settings, participants have less freedom in how they apply spatial memory, they have less external cues that normally 32 help them to move around or recall spatial settings, and problems might be encountered that do not occur in everyday life or the other way around. All tasks described above can be used in different environmental settings such as familiar or unfamiliar, hectic or calm, complex or simple and in emotionally disturbing (simulating emergency situations) or in passive and unexciting settings. This will improve ecological validity of spatial memory studies. 5. Conclusions and recommendations The outline of this review consisted of evidence for different forms of spatial memory and how these forms relate to different memory problems in everyday life, the everyday problems were classified, different factors that may lead to everyday spatial memory problems were described and finally different methods to assess everyday spatial memory were presented. Deficits in specific forms of spatial memory can be a result of age, gender, neurological damage, perceptual impairments, stress or mood. These factors can therefore lead to particular problems in everyday life, such as losing objects or getting lost yourself. In Table 1, we present an outline of different everyday spatial memory problems that can be divided into different groups of everyday problems and the related forms of spatial memory and underlying factors. This table clarifies how forms of spatial memory, underlying factors and specific everyday problems are interrelated. In chapter 2, we created groups of spatial memory problems that correspond to the same divisions, that is, if different problems are each large scale, long term and dynamic spatial memory problems; they are assigned to one group. With these groups, one problem may predict other spatial problems that are assigned to the same group. Table 1 confirms this assumption where for example ‘taking a longer route than necessary’ and ‘giving other people wrong route directions’ are assigned to the same group (dynamic-long term -large scale). These two problems also involve mostly similar components of spatial memory and similar groups of people may encounter these problems. Obviously, the content of this table and also the content of these groups should be tested and confirmed by future studies. One thing that leaps out in this table is that ‘age’ and ‘hippocampal damage’ are factors that may cause all everyday spatial memory problems. Whether some problems 33 occur less frequently than others or which problems have greatest impact on everyday life is not yet entirely clear. Again, future research should shed more light on this issue. Other factors, such as mood and visual impairments may cause more specific problems in everyday life. More knowledge about everyday spatial memory problems and about whether these problems fit into the groups and the table we have put forward, could perhaps contribute to improved spatial memory performance in elderly, impaired, male or female, and anxious people in different environments or during different situations. At present, the groups and Table 1 are developed based on independent spatial memory studies that are exceedingly dissimilar not just in the use of methods, settings and participants, but also in their aims. We suggest that an inventory should be made about everyday spatial memory problems for different groups of people. Surveys and questionnaires are suitable methods to accumulate a large amount of information from a large number of people (as such, including different groups of people) as long as the questions are detailed and simple. This review has shown that multiple components (and likewise specific everyday spatial memory problems) can be tested in natural settings using various methods. A strong advantage of measuring spatial memory in everyday settings is that spatial memory is measured as it is actually used in everyday life. However, a major and very important disadvantage is that the experimental conditions are mostly uncontrolled which leads to increased influence of confounding factors that might bring down the reliability and validity of the results. Furthermore, to study route learning or navigating in many different environments may not be very practical or attainable. These disadvantages of measuring in real-world settings are in fact the advantages of VE studies. VEs are completely controlled close-to-natural environments that can resemble every possible real-world setting without restrictions. It is therefore easy to create either familiar or unfamiliar environments. The only problem with VEs is that it is not completely clear to what extent behaviour in VEs can be generalized to behaviour in the real world. Several studies have revealed contradictory results about whether or not behaviour in VEs transfers to behaviour in real environments. The main restrictions that may prevent spatial memory performance in VEs to resemble spatial memory performance in the real 34 world are the small field of view and the inability to truly move while ‘walking’ around in a VE. However, making VEs more realistic has already proven to increase the generalizability of VE spatial memory performance. In addition, recent VE developments have made actual walking in a 360 degrees surrounding VE possible. Based on these findings and on the fact that a controlled experimental setting is essential to obtain reliable results, we strongly support the use of VEs in future everyday spatial memory research. 35 Everyday spatial memory problems Underlying factors Dynamic-short term-large scale Prospective / Retrospective Retrospective Static-short term-small scale Retrospective Age; HIPP damage; Monocular vision; Mood OLM Static-long term-small scale Retrospective Age; HIPP damage; Monocular vision; Mood CM Prospective Age; Gender; HIPP/PFC damage; Mood RL Static-long or short term-small to large scale Dynamic-short term-large scale Retrospective Age; PFC/HIPP damage; Blindness; Low vision Problems with estimating distances between buildings Taking a longer route than necessary CM; ALL; COO Static-long term-large scale Age; Gender; HIPP damage; Blindness; Mood RL; CM; ALL Dynamic-long term-large scale Prospective / Retrospective Prospective Giving other people wrong route directions Forgetting the route you followed earlier Pointing into wrong directions RL; CM; ALL; EGO RL Dynamic-long term-large scale Prospective Age; PFC/HIPP damage; Blindness; Low Vision Dynamic-short term-large scale Retrospective Age; PFC/HIPP damage; Low vision OLM; CM; ALL; EGO; COO Static-short term-large scale Prospective / Retrospective Age; HIPP damage; Monocular vision; Blindness; Mood Getting lost in a strange city Forgetting where you left your keys in a new room Forgetting where you left your keys in a familiar room Being unable to read or to understand a map Forgetting how you got somewhere Spatial memory components * RL; CM; EGO; ALL OLM Group of everyday problems Age; PFC/HIPP damage; Blindness; Age; PFC/HIPP damage; Blindness; Low Vision * RL = Route Learning; CM = Cognitive Map; EGO = Egocentric frame of reference; ALL = Allocentric frame of reference; OLM = Object Location Memory; COO = Coordinate coding Table 1: This table includes several spatial memory problems and shows which components of spatial memory may be involved, in which group that particular problem would fit, whether the problem concerns pro- or retrospective spatial memory and which underlying factors may have caused each problem. 36 REFERENCES master thesis ABRAHAMS, S., MORRIS, R.G., POLKEY, C.E., JAROSZ, J.M., COX, T.C.S., GRAVES, M. & PICKERING, A. 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