International Congress Series 1250 (2003) 261 – 274

Reference frames and cognitive strategies during navigation: is the left hippocampal formation involved in the sequential aspects of route memory? Simon Lambrey a,*, Se´verine Samson b, Sophie Dupont c, Michel Baulac c, Alain Berthoz a a

LPPA, Colle`ge de France-CNRS, 11 Place Marcelin Berthelot, 75005, Paris, France b URECA, Lille 3 University, Lille, France c EMI ‘‘Cortex Epilepsy’’, Salpeˆtrie`re Hospital, Paris, France

Abstract The precise role of the human medial temporal lobes (MTLs) in navigation is still keenly debated. Many studies in the literature have implicated either the right or both right and left MTLs in tasks requiring spatial memory. Notably, it has been hypothesised that the right human hippocampus is involved in navigation (e.g. topographical memory) while the left hippocampus is involved rather in processing the events that characterise our everyday lives (i.e. in episodic memory). The precise role of the left MTL, however, remains unclear. In the present paper, studies demonstrating the role of MTL structures in rodents and humans are reviewed. The potential involvement of the rat hippocampus in sequence memory is emphasised. Furthermore, the results of two studies investigating the neural basis of route memory in humans are discussed in light of the relevant literature. Notably, we will present the preliminary results of a neuropsychological study in virtual reality, suggesting that the left medial temporal lobe is involved in sequential aspects of route memory. Lastly, the following functional lateralization of the MTL is proposed over and above its involvement in navigation: the left MTL would be preferentially involved in memory for experienced relational information (sequential memory) while the right MTL would preferentially underlie inferential, holistic memory. D 2003 Published by Elsevier B.V. Keywords: Medial temporal lobe; Navigation; Route strategy; Sequential memory

* Corresponding author. Tel.: +33-1-44-27-13-86; fax: +33-1-44-27-13-82. E-mail address: [email protected] (S. Lambrey). 0531-5131/ D 2003 Published by Elsevier B.V. doi:10.1016/S0531-5131(03)00997-X

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1. Introduction A fundamental property of the primate brain is the ability to simulate internally planned actions and predict their consequences based on memory. In contrast to organisms whose behaviour is dictated by sensorimotor fixed strategies, this allows us to make decisions about the most appropriate action given our current goal. We have proposed the notion that the brain is a simulator and an emulator of actions, which can manipulate ‘‘cognitive strategies’’ using multiple, flexible, distinct, spatial reference frames to search for the optimal set of actions depending upon the goal and the context [1]. An interesting model of such internal mechanisms concerns spatial memory of travelled paths, e.g. remembering the route from our house to the office. In the present paper, we will first define route strategies as opposed to survey strategies. We will then report some findings concerning the role of the hippocampal formation in rodents, notably emphasising its potential involvement in sequence memory whatever the nature of the sequence, i.e. spatial or non-spatial. In a third part, we will review the literature on spatial memory in humans, and route memory in particular. Notably, we will present the preliminary results of a virtual reality study suggesting that the left medial temporal lobe (MTL) is involved in sequential aspects of route memory.

2. Route (egocentric) and survey (allocentric) cognitive strategies for spatial memory Two main strategies for memorising one’s trajectory, namely route and survey, are classically distinguished in behavioural studies of human spatial cognition [2,3]. Route strategy consists of memorising the spatial layout of the environment from the perspective of a ground-level local view (egocentric) and then remembering the sequence of the landmarks encountered and of the turns performed along the route, as well as the association between a given landmark and the subsequent direction taken. It can be called an ‘‘egocentric’’ strategy involving what has been called ‘‘topokinaesthetic’’ memory [4]. Psychophysical studies have revealed that route memory uses vestibular information about turns and self-motion and that the main variables describing locomotor trajectories are processed in distinct modules. For instance, there is a dissociation between memory for distance and memory for direction [5– 8]. Three main types of ‘‘topokinesthetic’’ variables could be processed in distinct neuronal subsystems: (1) rotations estimated by combining visual, vestibular and kinaesthetic cues, which are processed in the ‘‘vestibular cortex’’ [9]; (2) head direction, which is processed in the head direction cell system and (3) place, which is processed at the level of the hippocampus associated with self motion cues [10 –12]. In contrast to route strategy, survey strategy consists of evoking a map-like view of the environment (i.e. an allocentric view) and looking mentally at this map in order to take one’s bearings or locate oneself in the environment. Survey knowledge can be acquired either directly from a map or from navigation by representing sequential route knowledge in an object-like representation. Developmental studies support this hierarchical relationship between route and survey knowledge, demonstrating that children develop route learning before survey learning [2]. One key point is that, unlike route learning, which only allows one to follow previously travelled paths, the survey strategy allows one to find

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shortcuts and to infer new ways from one place to another. Tolman [13] was the first to describe this inferential characteristic of survey knowledge, showing that rats form ‘‘cognitive maps’’ based on spatial relationships between salient environmental cues and that such representations support flexible navigation behaviour (e.g. shortcuts). Interestingly, a third strategy has been proposed, which could be called an ‘‘architectural strategy’’ [14]. If, for instance, you think about the building in which you work and try to imagine where the office of a certain colleague is, you will probably have a kind of transparent inner perception of the whole building, keeping in mind only the general structure (i.e. architectural structure).

3. The rat hippocampus as a cognitive map: what is beyond? In 1971, O’Keefe and Dostrovsky [15] recorded ‘‘place cells’’ activity in the rat hippocampus. These neurones become active as animals move through specific regions in their environment, independently of the behaviour or the direction of the head (see Refs. [16 – 19] for recent reviews about place cells). Subsequently, O’Keefe and Nadel [20] proposed the theory of the rat hippocampus as a cognitive map. Moreover, lesions of the hippocampal formation in rodents induce permanent deficits in spatial orientation in a wide variety of situations in which animals are required to solve a task by using an allocentric representation of the environment (e.g. Ref. [21]). From that moment on, the rat hippocampus was thought to be specialised in spatial memory, although such a view has since been challenged [22,23]. However, too much emphasis would appear to have been placed on the so-called ‘‘cognitive map’’ function of the right MTL, disregarding its possible involvement in egocentric, sequential organisation of memory of travelled routes. Interestingly, models have emphasised the potential role of the hippocampal formation in encoding and retrieving sequences of events that compose episodic memories [24 –27]. Similarly, experiments in rodents have demonstrated a critical role of the hippocampus in memory for sequences of events [28] or of recently visited spatial locations [29,30], which can be related to route memory. On the other hand some authors [31,32] have shown that the rat hippocampus is essential for the acquisition and flexible, inferential expression of an orderly series of relationships between non-spatial items. For instance [32], rats learned a set of pair-wise ‘‘premises’’: A>B then B>C then C>D then D>E, where the rats were trained to select items to the left of the ‘‘>’’ over those on the right. Intact rats readily acquired the premises and, most importantly, could infer the appropriate transitive relationship between non-adjacent stimuli. Such an inferential capacity could be related to survey spatial knowledge that allows ones to infer shortcuts. Interestingly, the authors showed that, following hippocampal disconnection, rats learned the four premises but showed no capacity for inference about indirectly related items. Consistent with these results, Wallenstein et al. [26] argued that the hippocampus is most critically involved in learning and memory tasks in which discontiguous items must be associated, in terms of their temporal order or spatial positioning, or both. Asking whether the hippocampal formation underlies spatial memory or rather a ‘‘memory space’’, Eichenbaum et al. [33] reviewed many electrophysiological studies demonstrating that some of the properties of hippocampal neuronal firing patterns are inconsistent with the notion of a cognitive map.

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According to the authors, the notion of ‘‘place cells’’ would only illustrate, rather than define, the properties of hippocampal pyramidal cells. Eichenbaum et al. [33] argued that the regularity of experienced events determines the information encoded by hippocampal neurones. In addition, they proposed that some hippocampal neurones encode the temporal sequence in which a set of events compose particular behavioural episodes, while others encode the spatial and non-spatial regularities of the experience that are shared across different episodes (connection nodes). According to the authors, the prototypical event, sequence, and nodal representations could compose the memory space of interconnections in the hippocampus.

4. The importance of route strategy and the neural basis of egocentric spatial orientation 4.1. The neural basis of spatial orientation: a review Brain damage in humans may result in topographical disorientation, which can reflect the deterioration of distinct mechanisms (see Ref. [34] for review). In the neuropsychological literature there is, for instance, a clear dissociation between route and survey strategies. Notably, a dissociation has been claimed between, on the one hand, an impairment of the ability to recognise familiar landmarks, leaving the capacity to describe well-known routes relatively intact [35,36], and on the other hand, an impairment of the ability to describe routes with landmark recognition relatively unaffected [37,38]. Sometimes patients can also describe routes and recognise landmarks yet still lose their way because landmarks no longer convey directional information [39]. Because spatial disorientation is often a threat to the patient’s autonomy, the mechanisms and neural basis of spatial orientation have been extensively investigated using both neuropsychological and brain imaging paradigms. Recent brain imaging and neuropsychological studies in humans have suggested the involvement of a broad prefrontal and parieto-temporal network in navigation and spatial orientation (see Refs. [40 –43] for reviews), notably including the left prefrontal cortex, the medial and right inferior parietal cortex, the posterior cingulate cortex and the MTLs. To date, the MTL (including the hippocampus proper, the entorhinal, perirhinal and parahippocampal cortices) is the brain region that has received the most attention in this domain, yet its precise role still remains unclear. Since the report of case H.M. with bilateral MTL damage [44], the human hippocampus has been known to be important for episodic memory (i.e. retrieving the spatio-temporal context of everyday life events). However, Vargha-Khadem et al. [45] reported that, in addition to having impaired episodic memory, patients with early, selective, bilateral damage restricted to the hippocampus proper were unable to find their way around. Another study suggested that a lesion restricted to the parahippocampal gyrus could also entail topographic disorientation [46]. More recently, Teng and Squire [47] asked an amnesic patient to describe routes travelled either before or after the occurrence of bilateral damage to the medial temporal lobes. The patient was able to recall the spatial layout of the region where he grew up as accurately as control subjects,

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but had no knowledge of his current neighbourhood, to which he moved after he became amnesic. No such severe topographic disorientation was found in patients with unilateral MTL damage. However, a large number of neuropsychological studies have implicated the right medial temporal lobe in spatial memory of small-scale environments [48 – 53] or largescale environments [54 –56]. Moreover, several brain imaging studies have reported increased activity in the right hippocampus of subjects learning how to navigate through a large-scale environment [3,57], recalling previously learned routes [58,59] or navigating to a target place in a virtual maze [60,61]. By contrast, patients with left temporal damage have been shown to be impaired on tests of delayed recall of prose passages, recalling only fragments of the passage, whereas patients with right temporal damage perform as well as control subjects [62]. A similar dissociation between these two groups of patients was observed in tasks such as the learning and recall of word lists [63,64] and the recall of objects’ names [65]. Moreover, an activation specifically associated with retrieving the context of lifelike virtual reality events [66] or autobiographical real event memories [67,68] has been reported in the left hippocampus (see Ref. [69] for a review). Consistent with the literature cited above, it has been hypothesised that the right human hippocampus is involved in navigation (e.g. topographical memory) while the left hippocampus is involved rather in processing the events that characterise our everyday lives (i.e. in episodic memory) [56,70 – 72]. However, it should be emphasised that in some brain imaging studies the activation in the medial temporal lobe associated with navigation was not only on the right, but also on the left [3,57,58,60,61]. Furthermore, the extensive experience of spatial navigation of licensed London taxi drivers was shown to be associated with a significantly increased volume of grey matter in only two brain regions, namely the right and left hippocampi [73]. Interestingly, a recent lesion study in humans demonstrated that left medial temporal lobe lesions systematically affect the use of allocentric but not egocentric cues in various visuo-spatial memory tasks, suggesting that the hippocampal structures, and particularly the left, are crucial for allocentric, but not egocentric spatial memory [74]. Consequently, it is very likely that the human left hippocampus also plays a role in navigation. Below, we report the results of two studies supporting the hypothesis of an involvement of the left medial temporal lobe in route memory. These results are discussed in the light of the relevant literature. 4.2. Involvement of the left MTL in route memory: a brain imaging approach The results summarised in this section have been published elsewhere by Ghaem et al. [58]. We shall therefore consider only the main features of the study. Subjects were driven to a totally unfamiliar urban environment, in which they had to walk along a previously selected route of about 800-m in length. During navigation, they were asked to memorise the route and in particular seven prominent visual landmarks (a tower, a petrol station, a phone box, etc.). The day after this learning session and 4 – 6 h before positron emission tomography (PET) acquisition, subjects were trained to perform two tasks, which were repeated during the PET scan. In a task requiring mental simulation of routes, subjects had to mentally simulate navigation (i.e. to recall visual as well as sensorimotor mental images) between two landmarks, which were verbally indicated by the experimenter

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through earphones (departure point first, arrival point second). In a task requiring visual imagery of landmarks, subjects were instructed to mentally visualise a landmark upon hearing its name through the earphones and to maintain a mental image of it until they heard the name of another landmark 10 s later. Interestingly in the context of the present paper, when compared with visual imagery of landmarks, mental simulation of routes elicited activations in the left precuneus, the left insula and medial part of the left but not right hippocampal regions. The authors postulated that the medial part of the left hippocampal regions connect visuospatial and body position information to allow a coherent reconstitution of navigation. According to Maguire [72], activation of the left hippocampus in navigation tasks would rather reflect the processing of particular aspects of the context in which the events, such as navigation, are taking place. What makes the navigation task in the study by Ghaem et al. [58] different from the others referred to above (see Section 4.1)? In fact, subjects were instructed to mentally navigate between two landmarks along previously travelled routes, i.e. to adopt a pure route strategy. In contrast, the navigation tasks used in other studies required, most of the time, something more akin to survey knowledge. For instance, subjects had to connect spatial information acquired from navigation along two distinct routes [57] or had to freely navigate in a large-scale virtual environment before performing way-finding tasks [60]. It could therefore be hypothesised that both right and left hippocampal formations are involved in navigation, but in a different way: the right hippocampal formation could be involved in survey spatial knowledge while the left hippocampal formation could be involved in route memory. The way in which the left MTL is involved in route memory, however, remains unclear. 4.3. Involvement of the left MTL in sequential aspects of route memory: the preliminary results of a neuropsychological study The experimental set-up used in this study is derived from one we have described elsewhere [75,76]. Control subjects and unilateral MTL resection patients stood at the central point of a circular safety rail and were fitted with a virtual reality helmet (Fig. 1). They navigated five times through a large-scale virtual maze, following the same path each time (Fig. 2A). During each navigation, they started from the departure room (small room with two windows), went through seven crossroads that each had a different spatial layout, and then arrived in the final room where ‘‘END’’ was written on the wall. One landmark was placed at each crossroads. During navigation, subjects successively encountered a chair, a flower, a man, a clock, a ladder, a Christmas tree and a portrait (see Fig. 2B for an example of a crossroads with the corresponding landmark). During navigation, subjects were asked to memorise the path travelled, the landmarks encountered and the location of each landmark along the path. After each navigation, subjects were asked to draw the travelled path on a sheet of paper (see Fig. 3 for a synopsis of the paradigm). To prevent them from having visual feedback about the shape of the trajectory (i.e. survey perspective), subjects were told to close their eyes during this task. They were also asked to indicate (with a dot on the drawing) each time they remembered a landmark along the path and to name the landmark. The experimenter wrote down the landmarks in order of naming. An important result is that, although they could recall very well the list of landmarks seen

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Fig. 1. Experimental set-up. The standing subject was immersed in a virtual environment by means of a headmounted display. Translation in the corridor was imposed by the computer. The direction of the subject’s head was recorded using a magnetic tracking system. Custom-written software processed the data on the head angular position sent by the tracker and updated the corresponding visual image, providing the visual rotation components in the virtual corridor.

Fig. 2. Virtual environment. (A) Map of the virtual maze. (B) Graphic model of the virtual environment (example: view of the crossroads with the ladder). The direction to be taken at crossroads was signposted by green-coloured walls while all the wrong directions were signposted by red-coloured walls. The thick line represents the path followed by subjects.

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Fig. 3. Synopsis of the experiment. Subjects navigated along the path five times. After each navigation, they were tested on their memory for the route travelled using a map drawing task.

along the route, left temporal lobe (LTL) patients were significantly less accurate than control subjects in recalling the sequence of landmarks (Fig. 4), while the right temporal lobe (RTL) group’s performance was intermediate between that of the control and LTL

Fig. 4. Memory for the sequence of landmarks in control and patient groups. The inaccuracy of memory for the sequence of landmarks was expressed as the percentage of landmarks that were not correctly placed along the path during the map drawing path. Error bars are the standard error of the mean. * indicates significantly impaired relative to the control group ( p < 0.05).

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groups. LTL patients were also impaired relative to control subjects in memory for the association between a given landmark and the corresponding movement decision. Recently, Spiers et al. [56] used a large-scale virtual reality town in order to test the topographical and episodic memory of patients with unilateral MTL damage. After they had explored the town, subjects’ topographical memory was tested by requiring them to navigate to specific locations, to recognise scenes from the environment and to draw a map of the town. Following the topographical memory tests, subjects followed a route around the same town but now collected objects from two different characters in two different locations. Episodic memory for various aspects of these events was then assessed. The results showed that patients with right temporal damage were impaired on tests of topographical memory, whereas patients with left temporal damage were impaired on tests of context-dependent episodic memory. In particular, LTL patients were impaired relative to control subjects and to RTL patients in memory for the order in which objects were received from characters along a route. These findings are totally consistent with the preliminary results that are reported in the present paper, but Spiers et al. did not discuss a possible connection between such an impairment in LTL patients and the potential involvement of the left medial temporal lobe in route memory. Interestingly, Maguire et al. [54] showed that both LTL and RTL patients were impaired relative to control subjects in a task requiring memory for the sequence of landmarks along a route. In this study, subjects viewed the video presentations of two overlapping routes and were then tested on a route knowledge task. They were shown three photographs labelled ‘start’, ‘mid-point’ and ‘end’, respectively. Together with four additional landmark photographs, the task required ordering the landmarks in the correct sequence based on the routes seen in the video presentations. The important point is that the majority of the route knowledge trials involved between-route stimuli, and subjects therefore had to connect spatial information acquired from navigation along two distinct routes, i.e. to infer a new route from the two they had travelled. By contrast, in the present study and the study by Spiers et al. [56], subjects had to learn only one route and the task did not require any spatial inference. Hence, the impairment in the RTL group observed by Maguire et al. [54] could be explained by a potential involvement of the right medial temporal lobe in inferential spatial knowledge, e.g. survey knowledge. Consistent with this view, our results suggest that the left but not the right MTL is involved in memory for the sequence of landmarks encountered along a route during navigation, i.e. sequential spatial knowledge. One explanation for such a functional lateralization is that memory for the sequence of landmarks and memory for the landmark/movement associations each involved verbal encoding. Some studies have indeed suggested material-specific lateralization of brain involvement in memory processes, with greater left medial temporal lobe involvement for verbal material and greater right medial temporal lobe involvement for nonverbal material [62 – 65,77,78]. However, in the present study, LTL patients were impaired in recalling the temporal order in which the landmarks appeared during navigation, but not in recalling the landmarks encountered along the path (independently of the landmark location). Thus the impairment in memory for the sequence of landmarks observed in LTL patients cannot simply be explained by verbal difficulties, but rather suggests a specific involvement of the left MTL structures in sequence memory. It seems also possible that sequential spatial memory could rely on the coding of distal allocentric cues (such as, for example, ‘‘the

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ladder was just after the clock but well before the portrait’’), which seems to depend on the left hippocampal structures [74].

5. Conclusion The present paper supports the hypothesis that the right and left MTLs are each involved in navigation and large-scale spatial memory, but in different ways: the right MTL would be preferentially involved in survey spatial knowledge while the left MTL would be preferentially involved in route memory. Such a hemispheric asymmetry would, of course, be relative rather than absolute. Interestingly, the following functional lateralization of the MTLs can be postulated beyond their involvement in navigation: the left MTL would be involved in memory for experienced relational information (e.g. sequential memory, associative learning, route memory), while the right MTL would underlie all kinds of inferential memory (e.g. transitive inference, spatial inference, survey spatial knowledge). This view is consistent with the idea of Eichenbaum et al. [33] of the rat hippocampus as a ‘‘memory space’’ rather than a cognitive map (see Section 2), even if these authors did not mention any functional lateralization of the rat hippocampus in sequential versus inferential memory capacities. The absence of literature about hippocampal asymmetry in rodents could be due to the fact that this issue has not been addressed. Another explanation could be that brain asymmetry, which exists in various species, and notably in rodents, is more marked in primates, and therefore more visible in experiments involving human beings. Whatever the case, a hippocampal functional lateralization of this type in humans is totally consistent with the hypothesis of a more general brain asymmetry, with a left hemisphere bias for local processing and a right hemisphere bias for global processing [79 –83].

Acknowledgements This work was supported by SmithKline Beecham. The equipment was provided in part by the Centre National de Recherches Spatiales (CNES). We thank Pr. Roland Jouvent from Salpeˆtrie`re Hospital for allowing us to use space in his laboratory for installing this experiment. The authors wish to thank Michel-Ange Amorim, from UFR STAPS University of Orsay, and Manuel Vidal, from the LPPA, for advice on data analysis and precious comments on the manuscript, France Maloumian for the graphs and the engineering staff of the LPPA, Michel Ehrette, Ge´rard Krebs and Mohammed Zaoui, who contributed to this project.

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