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Deficits in egocentric-updating and spatial context memory in a case of developmental amnesia ab

a

a

ac

A. Gomez , S. Rousset , C. Bonniot , A. Charnallet a

& O. Moreaud

ac

LPNC, CNRS, UMR 5105, Université Grenoble Alpes, Grenoble, France

b

ESPE, Centre de Neurosciences Cognitives, CNRS, UMR 5229, Université Claude Bernard Lyon 1, Bron, France c

Pôle de psychiatrie et Neurologie, CMRR & Neuropsychologie, CHU de Grenoble, Grenoble, France Published online: 03 Mar 2014.

Click for updates To cite this article: A. Gomez, S. Rousset, C. Bonniot, A. Charnallet & O. Moreaud (2015) Deficits in egocentric-updating and spatial context memory in a case of developmental amnesia, Neurocase: The Neural Basis of Cognition, 21:2, 226-243, DOI: 10.1080/13554794.2014.890730 To link to this article: http://dx.doi.org/10.1080/13554794.2014.890730

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Neurocase, 2015 Vol. 21, No. 2, 226–243, http://dx.doi.org/10.1080/13554794.2014.890730

Deficits in egocentric-updating and spatial context memory in a case of developmental amnesia A. Gomeza,b*, S. Rousseta, C. Bonniota, A. Charnalleta,c and O. Moreauda,c a

LPNC, CNRS, UMR 5105, Université Grenoble Alpes, Grenoble, France; bESPE, Centre de Neurosciences Cognitives, CNRS, UMR 5229, Université Claude Bernard Lyon 1, Bron, France; cPôle de psychiatrie et Neurologie, CMRR & Neuropsychologie, CHU de Grenoble, Grenoble, France

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(Received 15 February 2013; accepted 22 December 2013) Patients with developmental amnesia usually suffer from both episodic and spatial memory deficits. DM, a developmental amnesic, was impaired in her ability to process self-motion (i.e., idiothetic) information while her ability to process external stable landmarks (i.e., allothetic) was preserved when no self-motion processing was required. On a naturalistic and incidental episodic task, DM was severely and predictably impaired on both free and cued recall tasks. Interestingly, when cued, she was more impaired at recalling spatial context than factual or temporal information. Theoretical implications of that co-occurrence of deficits and those dissociations are discussed and testable cerebral hypothesis are proposed. Keywords: hippocampus; parietal; spatial memory; allocentric; episodic memory

Episodic memory is defined as the memory of an event within its spatiotemporal context (Burgess, Becker, King, & O’Keefe, 2001; Davachi & Wagner, 2002; Teyler & DiScenna, 1986). Such memories crucially encompass a phenomenological experience defined as a feeling of selfawareness and a mental travel in space and time (Tulving, 2002, 2005). Several studies suggest that episodic memory is impaired in the case of hippocampal damage or dysfunction, resulting in profound amnesia (Cermak, 1984; Guillery-Girard et al., 2006; Rosenbaum et al., 2005; Vargha-Khadem, 1997). One major source of evidence toward the involvement of the hippocampal formation in context-dependent memory comes from the study of several patients with developmental amnesia (Baddeley, Vargha-Khadem, & Mishkin, 2001; Spiers, Maguire, & Burgess, 2001; Vargha-Khadem, 1997). Building on influential models of spatial functions (O’Keefe & Dostrovsky, 1971; O’Keefe & Nadel, 1978) several theories of episodic memory suggest that the hippocampal formation is particularly relevant to process the spatial context of events (Burgess, Becker, et al., 2001; Burgess, Maguire, Spiers, & O’Keefe, 2001; Byrne, Becker, & Burgess, 2007; Kentros, 2006; Moscovitch & Nadel, 1998; Moscovitch et al., 2005). This structure could bind the different elements of an event and, thus, ensure a coherent reconstruction of the event at retrieval by providing a spatial scaffold (Burgess, Becker, et al., 2001; Burgess, Maguire, et al., 2001; Byrne et al., 2007; Moscovitch et al., 2005). Following early spatial memory theories (O’Keefe & Dostrovsky, 1971; O’Keefe & Nadel, 1978), the spatial context might be processed within an allocentric representation (i.e., coding for objet-to object *Corresponding author. Email: [email protected] © 2014 Taylor & Francis

relations and centered on aspects of the external environment; Burgess, 2006, 2008). To test this hypothesis, King, Trinkler, Hartley, Vargha-Khadem, and Burgess (2004) assessed the context memory of Jon, a developmental amnesic patient, whose memory performance has been extensively studied (Baddeley et al., 2001; Duzel, Vargha-Khadem, Heinze, & Mishkin, 2001; Spiers, Burgess, Hartley, VarghaKhadem, & O’Keefe, 2001; Vargha-Khadem, 1997) and who presents deficits in recollection processes with preserved familiarity capacities. The authors provided evidence that following a relatively naturalistic (virtual reality) encoding phase of an event, Jon was impaired in a forced-choice recognition test, requiring the association of an object to its location or of an object to a person. Jon was in the normal range on a mere object recognition task, and he presented a deficit to associate a “place” (i.e., spatial element “where”) and a “person” (i.e., factual element “what”) to an object. Jon’s equal impairments in retrieving spatial and nonspatial context of an event (e.g., the person who gave the object) is unexpected, given the core role devoted to spatial processing in explaining episodic memory deficits. In contrast, spatial impairments in Jon (King, Burgess, Hartley, Vargha-Khadem, & O’Keefe, 2002; King et al., 2004; Spiers, Burgess, et al., 2001) and in other amnesic patients (Bird et al., 2011; Buckner & Carroll, 2007; Holdstock et al., 2000) have been taken as evidence of the link between episodic and spatial functions. Although pure visuospatial object-location abilities (i.e., assessed with matching tasks based on retinotopic self- to objectlocation which are defined as iconic-egocentric tasks) are

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Neurocase preserved in amnesia, spatial memory is impaired whenever the object-location tasks includes a perspective shift between encoding and test. These results support the existence of a functional relationship between episodic and spatial functions through their common reliance on allocentric coding per se (Byrne et al., 2007; Moscovitch et al., 2005). From a neuroanatomical perspective, functional magnetic resonance imaging (fMRI) studies have revealed that in humans certain forms of allocentric processing are supported by a larger network of regions including the parietal, the retrosplenial and the parahippocampal cortex (e.g., Aguirre, Detre, Alsop, & D’Esposito, 1996; Committeri et al., 2004; Galati et al., 2000; Vallar et al., 1999; Zhang & Ekstrom, 2013; for review Galati, Pelle, Berthoz, & Committeri, 2010). Furthermore, several lines of evidence converge to suggest that the hippocampus is not always involved or necessary in allocentric processing (Aguirre et al., 1996; Bastin et al., 2013; Bohbot et al., 1998; Committeri et al., 2004; Galati et al., 2000; Zhang & Ekstrom, 2013). Bohbot and colleagues (1998) reported that patients suffering from unilateral hippocampal lesions performed like controls in an adapted version of the Morris water maze task assessing some forms of allocentric representation. The parahippocampal cortex appeared responsible for these residual functions (Bohbot & Corkin, 2007). Parahippocampal electrophysiological recordings confirmed allocentric (environment-centered) specific neural activity (Bastin et al., 2013). With regard to spatial processing, a distinct line of research has demonstrated that the hippocampal structure is crucially involved in self-motion processing in rodents (McNaughton, Battaglia, Jensen, Moser, & Moser, 2006; Redish & Touretzky, 1997; Smith, Darlington, & Zheng, 2010; Terrazas et al., 2005; Whishaw, McKenna, & Maaswinkel, 1997; for contradictory results see Alyan & McNaughton, 1999; Shrager, Kirwan, & Squire, 2008). In human, spatial context can also be processed through egocentric-updating representation (i.e., based on selfmotion information, called idiothetic cues, Farrell & Robertson, 1998; Frances Wang & Simons, 1999; Wang & Spelke, 2000). Egocentric-updating rely on self-motion information. These cues are relevant for spatial orientation without vision or audition. When both cues are available, the use of allothetic cues (i.e., external landmarks) becomes possible. Coherently with animals study, patients with hippocampal lesions fail to point toward the origin of a path in the dark (Philbeck, Behrmann, Levy, Potolicchio, & Caputy, 2004; Wiener, Berthoz, & Wolbers, 2011; Wolbers, Wiener, Mallot, & Buchel, 2007; Worsley et al., 2001), suggesting that the hippocampi may play a specific role in egocentric-updating. Nevertheless, the human parietal lobe is also clearly involved in egocentric referencing and egocentric navigation (Bremmer, 2011; Nitz, 2009). In rodents, the posterior parietal cortex

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(PPC) is thought to play a role in mnemonic processing of idiothetic spatial representations (based primarily on head direction information); but no study has previously demonstrated a sole involvement of the PPC for purely idiothetic process in humans (Kesner, 2009). Among parietal areas, the retrosplenial cortex of animals has been involved in head-direction processing (Cho & Sharp, 2001; Epstein, 2008; Maguire, 2001; Vann, Aggleton, & Maguire, 2009) as well as in idiothetic information and path integration processing (Redish & Touretzky, 1997; Wiener & Taube, 2005). In humans, the main function hypothesized for the retrosplenial structure is the transformation of egocentric-parietal representation in allocentric ones and vice versa (Byrne et al., 2007) for long-term memory storage. More broadly, the interplay between episodic and spatial functions possibly extends beyond the hippocampal structures to adjacent cortex (entorhinal, retrosplenial, parahippocampal) and even parietal regions (Buckner & Carroll, 2007; Buzsáki & Moser, 2013; Spreng, Mar, & Kim, 2009). In fact, parietal atrophies in developmental amnesia are not exceptional and might contribute to the classically observed pattern of memory deficits (Adlam, Vargha-Khadem, Mishkin, & de Haan, 2005; Isaacs et al., 2003; Vargha-Khadem, 1997; Vargha-Khadem et al., 2003). A whole-brain analysis of volumetric data in a large group of 10 developmental amnesic patients revealed several brain abnormalities, reflected in a reduction of gray-matter density in the hippocampus, thalamus, and basal ganglia (bilaterally) and, most importantly, in the right retrosplenial cortex (Vargha-Khadem et al., 2003). Surprisingly, once corrected for multiple comparisons, the retrosplenial cortex and the caudate remained significantly atrophic in developmental amnesic patients. Parietal atrophy is also frequently encountered in the case of acquired hippocampal reduction, after carbon monoxide poisoning (35% of patients, Caine & Watson, 2000) or after epileptical surgery as for patient HM (Salat et al., 2006). In several cases (Bastin et al., 2004), this parietal atrophy was observed several years after focal hippocampal lesions and could reflect a specific functional link between hippocampal and parietal structures. Hence, these results suggest that if the parietal areas thinning contribute to developmental amnesia, it might be through a disruption of the cooperation with atrophic mediotemporal structure. In fact, many fMRI studies reported parietal involvement during episodic memory tasks (Cabeza, 2008; Cabeza, Ciaramelli, & Moscovitch, 2012; Cabeza, Ciaramelli, Olson, & Moscovitch, 2008) with a key evidence provided by the reports of a decrease in the vividness and amount of detail in free recall of patients with bilateral parietal lobe lesions (Berryhill, Phuong, Picasso, Cabeza, & Olson, 2007). In accordance with these findings, recent proposal suggest that the link between episodic memory and spatial

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processing is neither restricted to the allocentric processing nor necessarily centered on the hippocampi. Instead, an important role could be played by egocentric-updating as it determines the translation process necessary for the firstperson mode retrieval to occur (Crawley & French, 2005). Egocentric-updating representation is suggested to participate in episodic memory functioning, given its characteristics (i.e., self-centered, integrating self-movement over time, Cerles & Rousset, 2012; Gomez, Rousset, & Baciu, 2009; Gomez, Rousset, & Charnallet, 2012). Gomez et al. (2009, 2012) proposed to add a memory property to the Byrne et al. (2007) model. In Byrne, Becker, and Burgess model, an event perceived in an egocentric-parietal reference frame is translated into an allocentric hippocampal reference frame for long-term memory storage. During retrieval, the allocentric trace is reactivated and translated back into an egocentric perspective. By adding a memory to the translation system, Gomez and colleagues provide a mechanism to disentangle an imaginary perspective from a real episodic memory. If the system memorizes the initial transformation (from the egocentric to the allocentric reference frame), then, at the time of retrieval, it will be faster and easier to re-create the initial egocentric perspective. Memorizing the initial translation (i.e., egocentric-updating during learning) will then allow the re-creation, during recall, of the specific point of view experienced at learning. The egocentricupdating proposal further suggests that eliciting a feeling of autonoetic consciousness, this ability to project oneself in the past (Tulving, 2002; Wheeler, Stuss, & Tulving, 1997), arises from this fluency in reinstating a specific egocentric perspective. In favor of the egocentric-updating hypothesis, Gomez et al. (2012) have shown that MR, who suffers from bilateral hippocampal amnesia, also presents a co-occurrence of episodic memory and egocentric-updated processing deficits without allocentric processing deficits. MR was preserved in an immediate allocentric spatial processing when it did not involve egocentric-updating during the learning phase. The aim of the present investigation is to provide further behavioral evidence of the link between episodic and spatial functions by assessing spatial processing in DM, a patient suffering from developmental amnesia resulting from a perinatally acquired bilateral hippocampal pathology. We used an object-location rotation task and a path reproduction task (based on Gomez et al., 2012) to assess DM’s immediate spatial recall abilities. We predicted a selective deficit of egocentric-updating processing in tasks where processing is highly dependent on idiothetic information. Moreover, we predicted the preservation of allocentric processing when it operates from allothetic information only, contrary to the prediction that can be drawn from theories supposing a dysfunction of the allocentric processing per se. To investigate further the link

between spatial and episodic memory processing, we also assessed DM’s anterograde episodic memory by using an ecological and controlled paradigm focusing on the “what”, “where”, “when” components of free and cued recall. We predicted that, as a result of a failure of egocentric-updating processes, DM would be severely impaired in recalling “where” elements when tested in conditions preventing compensatory process.

1. Materials and methods 1.1. Case description DM is a right-handed young woman, who was 31 years old at the time of testing (April 2010). After a normal birth, she presented on the fourth day and for several days a partial epilepticus status with right-sided convulsions, requiring a 3-week stay in intensive care unit. She never presented seizures again and has not been treated for epilepsy, nor has she had any medical treatment. DM presented a slight developmental retardation: walking was acquired at the age of 18 months (probably related to osteoarthritis of the hip diagnosed at 2 years old) and spoken language at 2 years. There is no neurological history until she reached the age of 5, when memory impairments were first noted at her entrance into a mainstream school. Her schooling was difficult, and new learning was very slow, effortful and required many repetitions. After several years, she managed to obtain a vocational training certificate as a beautician. Since early childhood, DM has been complaining of memory disorders leading to severe learning difficulties and to frequent omissions especially in prospective memory. In addition, she has always struggled to find her way, to learn routes or itineraries. These impairments have severely handicapped her in her professional life.

1.2. Control group Ten women matched on age (M = 26.4, SD = 4.5), education level and on estimated performance (IQ, Raven matrix, M = 100, SD = 10.4) were recruited via an announcement in a neuroscience experiment mailing list participated for a 50 euros compensation.

1.3. Neuropsychological examination DM’s performance on psychometric tests assessing memory function is presented in Table 1 (and includes general memory, recall and delayed test, recognition, short-term and procedural memory performance). On the Weschler Memory Scale-revised (WMS-R, Wechsler, 2001), DM was impaired especially on recall and on delayed memory tests. Verbal long-term memory was further assessed by a selective reminding test with free and cued recall (RL/RI 16,

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Table 1. Neuropsychological evaluation of DM’s memory functions.

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Part A WMS-R Delayed Verbal Memory Delayed Visual Memory General Memory Immediate Memory Working memory Free recall and cued recall RL/RI16 (Van der Linden et al., 2004) First trial: Free recall Total free + cued recall Second trial: Free recall Total free + cued recall Third trial: Free recall Total free + cued recall Recognition Hits False recognitions Delayed free recall Total Delayed free + cued recall Rivermaid Behavioral Memory Test (Wilson et al., 1985)

69 75 67 73 91

(pc (pc (pc (pc (pc

2) 5) 1) 4) 27)

(100 ±15)

5/16 (−2.33)* 8/16 (1 pc)

(8.48 ± 2.18)

3/16 (−3.88)*** 9/16 (1 pc)

(9.90 ± 2.27)

6/16 (−3.18)** 10/16 ( 0.5, Figure 4). This dissociation (p < 0.05) between the two conditions suggests that DM has trouble updating objects’ position relative to her orientation but has no difficulties in maintaining the relative position of different objects during this short period of time. This functional dissociation between the rotation and no rotation conditions suggests that DM’s deficit arises from an inability to update her self-motion orientation in space, rather than to code for object-locations over short delays. In the path reproduction task, results indicate that DM is impaired in the self-no-vision and in the self-vision encoding conditions compared to the CG (ps < 0.05) but is unimpaired in the experimenter encoding condition. *

80

Absolute error angle

70 60 50 40 DM

30 20 10

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Rotation

5 **

4 Corresponding Z-score

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1.5.3. Immediate spatial tasks results (Figures 3 and 4, Table 4)

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3 2 1 0 –1 –2

*

Figure 3. Object-location rotation task results. (Top) Overall error size in degrees for DM and the control group in each encoding condition (1, self-no-vision; 2, self-vision; 3, experimenter) on a drawing reproduction task. For the control group, the mean score is shown by the bar, and error bars indicate the standard error. Notes: *indicates effect of encoding in the control group. (Bottom) Corresponding Z-scores derived by comparing DM to the control group. The dashed line shows T = 2.26, *over bars indicate significant deficits, *over between bars indicate statistically significant dissociation between conditions. Overall *p < 0.05, **p < 0.01, ***p < 0.001.

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Number of cued elements correctly recalled

14 12 10 8

DM

6

CG

4 2 0 When

What

Where

–2

*

–4 Corresponding Z-score

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***

–6 –8

*

–10 –12 –14 –16 ***

–18 *** ***

Figure 4. Episodic memory task results: (left) plotted performance on free recall and on the right, performance on cued recall. (Top) Average number of elements freely recalled, or correctly recalled when cued respectively, for DM and the control group according to the components: (1) temporal, when; (2) factual, what; (3) spatial, where. For the control group, the mean score is shown by the bar, and error bars indicate the standard deviation. Notes: *effect of the component in the control group. (Bottom) Corresponding Z-scores derived by comparing DM to the control group. The dashed line shows T = 2.26, *over bars indicate significant deficits, *between bars indicate statistically significant dissociation between conditions. Overall *p < 0.05, **p < 0.01, ***p < 0.001.

Moreover, there is a dissociation between these tasks both on angular and on distance errors (ps < 0.05, Figure 4 and Table 4). In the path reproduction test, DM is impaired when she needs to track her body position in the Table 4.

Path reproduction task results.

Self-vision Self-no vision Experimenter

DM

CG

344*** 3.85*** 2.24

1.95 ± 0.38 2.09 ± 0.48 2.07 ± 0.49

Notes: Mean absolute distance error in meters for DM and the control group (CG, standard error in parentheses) according to the encoding condition: (1) self path production with vision, (2) self path production without vision, and (3) experimenter production of the path. ***indicates p < 0.001 significant deficits.

environment (i.e., on the basis of idiothetic information), but not when she can encode the path on the basis of the external information (i.e., on the sole basis of allothetic information). DM’s failure in the self-vision condition may be interpreted in two ways. First, the self-vision condition can be performed on the sole basis of allothetic information, and DM fails in this condition because processing allothetic information alone is less efficient than the use of both allothetic and idiothetic information. Alternatively, to succeed in the self-vision condition, the idiothetic information may be compulsory (even if both idiothetic and allothetic information are available) in order to update ones’ coordinate, track the path, and reproduce it. Hence, allothetic information may serve as additional source of information but would not be sufficient to solve the task, which would explain DM’s failure in the task. This

Neurocase latter hypothesis seems more likely given the similarity of DM’s results in the vision and no vision condition.

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1.5.4. Episodic memory task To assess the “what-where-when” components of episodic memory, we designed a new episodic memory task. Using a first appointment (Session 1) as an ecological reference event, we assessed on a subsequent appointment (Session 2) participant’s free and cued recall of this event. This procedure provides an experimental naturalistic and incidental episodic memory test. Although difficult to apply in standard neuropsychological evaluation, this task presents three advantages compared to other episodic memory tests: (1) it is an ecological episodic autobiographical memory test; (2) it is an experimentally controlled task, as the experimenter controls what is learned; (3) it assesses incidental learning, as the participant is not informed that the event will have to be recalled. 1.5.4.1. Encoding phase. On a prior appointment, participants performed different tests (digit span, money standardized road map test, left–right orientation test, rotation test, 3D joystick-computer test, track test, etc.) in different rooms and with different experimenters. 1.5.4.2. Test phase. Participants’ memory of this appointment was tested by means of a free and a cued recall task. Testing occurred after 2 weeks (±2 days) in a different room to prevent objects’ recognition or familiarity to provide additional help. Free recall instructions were built on the basis of TEMPau recall instructions (Piolino, 2003; Piolino, Desgranges, & Eustache, 2000). Participants were instructed to recall the last appointment at the hospital. They were asked to describe the events as accurately as possible and to locate them in space and time. They were required to describe the circumstances and events in details, and more specifically: (1) what happened (including who was present); (2) the location of the event (where), and (3) when it happened. Each recall was taped and then transcribed in text. Participants’ production was quoted by two experimenters and assigned to one of the three following categories: “what”, “where”, or “when” elements. Given the recall of participants, two additional categories were created: (1) “inner thoughts, feelings,” even though the veracity cannot be controlled for this category; and (2) intrusions. Cued recall questions were built following the methodology used by Adlam, Patterson, and Hodges (2009) to assess episodic memory in semantic dementia patients (see Figure B, supplementary materials). Participants had to answer specific questions about the event: 14 questions were proposed for each category (“what”, “where”, and “when”).

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1.5.5. Episodic memory results (Figure 5) Friedman tests were conducted on the control group as responses did not follow a Gaussian curve. In the free recall task, the control group showed a significant effect of category [χ2(2, 10) = 15.84, p < 0.001]. More factual elements (“what”, M = 23.1, SD = 5.15) were spontaneously recalled than spatial (“where”, M = 11.6, SD = 5.13) or temporal ones (“when”, M = 10.1, SD = 2.33, [χ2(1, 10) = 10.00, p < 0.001]). An effect of the category was also present for controls in the cued recall task [χ2(2, 10) = 7.94, p < 0.01] with fewer temporal than factual elements retrieved, and fewer factual than spatial elements retrieved (Figure 5). This suggests that the previous advantage of “what” elements reflects a tendency to spontaneously recall factual elements rather than spatial and temporal ones. Concerning DM, in the free recall task, she is overall severely impaired compared to the CG (p < 0.05) on free recall of the previous meeting, as she is able to report only 19 relevant elements (all categories pooled, including inner thoughts and details). She also pathologically reports nine events or elements that did not occur (p < 0.001). More specifically, she presents pathological results in the “what” (nine elements) and “inner thoughts and feeling” (one element) components (ps < 0.05), and borderline results on the “where” (two elements, T = −1.80, p = 0.1273),4 and “when” (six elements, T = −1.60, p = 0.1441) components. There is no significant dissociation between the performance in each category. In the cued recall task (Figure 5), DM was severely impaired on spatial (“Where”, p < 0.001) and factual (“What”, p < 0.001) information. On cued recall of temporal elements, effect was marginal (“when”, T = 2.16). It is possible that the present condition lacks sensitivity on the temporal component as suggested by both the near floor performance of controls and the null score of DM. Hence, if the present results do not allow any conclusions, a more sensitive task could presumably show an impairment of DM’s temporal context memory, in accordance with previous data indicating the involvement of hippocampal areas in temporal context memory (Downes, Mayes, MacDonald, & Hunkin, 2002; Howland, Harrison, Hannesson, & Phillips, 2008; Kesner, Gilbert, & Barua, 2002; Manns, Howard, & Eichenbaum, 2007; Mayes et al., 2001; Shimamura, Janowsky, & Squire, 1990). Interestingly, in this task, a functional dissociation appeared between DM’s profound impairment to recall cued spatial elements compared to her impairment on cued factual elements (p < 0.001). She was also more impaired in cued recall of factual than temporal elements (p < 0.05). The presence of a severe deficit in both free and cued recall of this episodic memory task confirms the

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160 140 120 100 80 60 40 20 0 Self-no vision

Experimenter

Self-vision

5

* * * * * *

Corresponding Z-score

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6

4 3 2 1 0 * *

Figure 5. Trajectory reproduction task angle error results. (Top) Overall error size in degrees for DM and the control group in each encoding condition (1, self-no vision; 2, self-vision; 3, experimenter) on a drawing reproduction task. For the control group, the mean score is shown by the bar, and error bars indicate the standard error. Notes: *indicates effect of encoding in the control group. (Bottom) Corresponding Z-scores derived by comparing DM to the control group. The dashed line shows T = 2.26, *over bars indicate significant deficits, *between bars indicate statistically significant dissociation between conditions. Overall *p < 0.05, **p < 0.01, ***p < 0.001.

neuropsychological evaluation results (e.g., selective reminding test with free and cued recall or TEMPau test) and shows that on recent events learned incidentally, DM is impaired when the information tested is irrelevant to her autobiography and was not rehearsed. DM presents a functional dissociation between her recall of spatial and factual elements: she truly lacks the ability to recall the spatial context of past events from her life. This dissociation is not present in free recall but control participants greatly differ on their spontaneous recall of spatial elements (as a reminder, M = 11.6 and SD = 5.15). The cued recall test is very interesting as it prevents her from using compensatory strategies and reduces the variance in the control group (leading to easy and steady reports of many spatial aspects, e.g., body position and spatial elements in controls only).

2. General discussion This study presents the case DM, a severely amnesic patient suffering from perinatally acquired bilateral damage to the hippocampal formation, associated with posterior parietal atrophy. The purpose of this study was (a) to link her amnesia to her performance in egocentricupdating spatial tasks and (b) to explore, by using a naturalistic incidental episodic task, her ability to recall “what”, “where”, and “when” components of an event episode. Unsurprisingly, DM is severely impaired on the experimental episodic recall task as expected in developmental and acquired amnesia (Baddeley et al., 2001; Duzel et al., 2001; Spiers et al., 2001; Vargha-Khadem, 1997). This case study shows that developmental amnesia can result in an impairment in the recall of context elements. With a cued recall procedure, we provide evidence that DM fails to retain an episode and that she fails to a greater

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Neurocase extent to retain its spatial context. Concerning the factual/ spatial dissociation, previous experiment with the patient Jon failed to show such a dissociation between spatial context elements (tested in a “place condition”, where subjects had to decide which of two presented objects had been previously seen in the depicted spatial context) and factual context elements (tested in a “person condition”, where subjects had to choose the correct association between an object and a character, independent location, King et al., 2004). We suggest that contamination by familiarity processes could account for Jon’s results in the forced-choice recognition task. Indeed, familiarity processes can be involved even when solving an inter-item associative recognition, as these items can be unitized during encoding (Jäger & Mecklinger, 2009; Piekema, Rijpkema, Fernández, & Kessels, 2010). The degree of unitization of different exemplar of the same item such as an object (i.e., object recognition task) is stronger than degree of unitization across items (i.e., object-place, object-person associative recognition task). So, insofar as less familiarity is engaged in an associative recognition test than in an item recognition test, this could explain why Jon is more impaired in the latter. Nevertheless, familiarity resulting from unitization across items could determine forced-choice recognition performance. This involvement of familiarity would contribute to the equivalence of performance for spatial (object-to-location test) and nonspatial contextual elements (object-to-person test). By using a recall procedure, our test prevents contamination by familiarity processes and assesses pure recollection process with no contamination by familiarity processes. This report of a compelling dissociation (between spatial context and factual components of the episodic memory) in developmental amnesia was (1) expected given previous knowledge gained from other research fields (behavioral, animal, imaging) and (2) in agreement with most theories of episodic memory, which suggest that the neural network encompassing the hippocampal formation provides a spatial context to an episode (Bird & Burgess, 2008; Burgess, Becker, et al., 2001; Byrne et al., 2007; Moscovitch & Nadel, 1998; Moscovitch et al., 2005). The preservation of DM’s allocentric spatial processing might seem more surprising, given previous reports of some forms of allocentric deficits in focal bilateral hippocampal amnesia (Holdstock et al., 2000; King et al., 2004). Those observations have previously supported theories suggesting a specific role of hippocampal formation in providing the spatial context of episodic memory (Bird & Burgess, 2008; Burgess, Becker, et al., 2001; Byrne et al., 2007; Moscovitch & Nadel, 1998; Moscovitch et al., 2005). In the path reproduction task, we observed that the patient with developmental bi-hippocampal amnesia associated to parietal atrophy is normal when she has to reproduce a trajectory performed by the experimenter. It indicates

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that she is quite able to use an allocentric representation based on external landmarks alone. Alternatively, she may also be able to use some forms of allocentric spatial updating in order to imagine herself performing the path in the environment (Farrell & Robertson, 1998; King et al., 2002). However, King et al. (2002) previously showed that such a spatial updating may be impaired in patients with bilateral hippocampal lesions. The use of this simulation process is thus here unlikely, and even if it had to play some role it would depend on an unimpaired allocentric coding. In the present case, we can conclude, from the preservation in this experimenter path reproduction condition, that bilateral hippocampal areas appear unnecessary to form an allocentric representation of a path based on external landmark information processing. Our report argues in favor of research which suggests that the hippocampus might not be necessary for all forms of allocentric spatial coding. In rodents, grid cells or border cells located in entorhinal cortex appear sufficient to perform many allocentric computations (Buzsáki & Moser, 2013; Moser, Kropff, & Moser, 2008). In humans, previous lesion studies have already suggested that humans with unilateral or bilateral hippocampal lesions may present preserved allocentric performance, and residual performance could be supported by parahippocampal areas (Bastin et al., 2013; Bohbot & Corkin, 2007; Bohbot et al., 1998b; Zhang & Ekstrom, 2013). The impairment of DMs’ immediate spatial abilities (without mental rotation or left–right orientation impairments) was also expected. Such a pattern of results is congruent with previous reports of immediate spatial memory deficits in patients with amnesia but has not been reported hitherto in the case of developmental amnesia (Buckner & Carroll, 2007; Holdstock et al., 2000; King et al., 2002, 2004). Congruently, DM presented a deficit in the path-encoding task without vision (i.e., idiothetic only). In the very same vein, DM was also impaired in the object-location rotation task without vision (i.e., idiothetic only) but not in the object-location memory task performed without rotation. Because the no-rotation condition was easier than the rotation condition, a nonlinear effect of difficulty could have accounted for these results, such that DM’s performance could fall much more dramatically than controls’ performance as difficulty increases. However, insofar as the path reproduction task conditions were of equivalent complexity for control participants and as results also demonstrate a specific deficit in egocentric updating based on idiothetic information in DM, such an interpretation remains unlikely. Patients with developmental amnesia could thus be impaired in updating egocentric representations while forms of allocentric and egocentric representations based on allothetic information might be preserved. If we now consider the neuronal structure involved in the observed spatial deficits, some studies on path integration have reported similar results in patients with acquired

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bilateral hippocampal amnesia (Gomez et al., 2012; Philbeck et al., 2004; Worsley et al., 2001). However, the parietal atrophy associated to bi-hippocampal amnesia could be responsible for the observed deficits (Teng & Squire, 1999). In particular, the retrosplenial areas which are often atrophic in developmental amnesia may be wellsuited to account for such deficits (Isaacs et al., 2003). Posterior parietal areas are fundamental to updating of egocentric information. Indeed, a subtype of topographical disorientation in the well-known taxonomy of Aguirre and D’Esposito (1999), namely the heading disorientation (i.e., an incapacity to draw allocentric information from egocentric information) is related to lesions in these areas. In fact, Maguire (2001) and Vann et al., (2009) have further reported that in fMRI studies parietal and retrosplenial areas were involved during navigation process. Hence, if indeed parietal-retrosplenial atrophies are not rare in developmental amnesia, and present in DM’s, this is the first report of such egocentric-updating deficits in this pathology to our knowledge. If clear-cut conclusions about the underlying neural structures must await further experimentations, we suggest that if the parietal areas thinning contribute to developmental amnesia in general and to DM’s spatial deficits in particular, it might be through a disruption of the cooperation with atrophic medio-temporal structure. Moreover, because parietal atrophies are frequent in developmental amnesia, they may also contribute more widely to the classically observed pattern of memory deficits. Hence, this parietal thinning clearly raises an interesting issue about the role of (1) parietal involvement and (2) parieto-temporal network involvement in episodic memory deficits of developmental amnesics. In fact, several theoretical hypotheses have already been formulated on the role of the parietal lobe in episodic memory. It has been envisaged to serve as an episodic buffer, a type of WM (Baddeley, 2000), providing an assessment of memory signal strength, as a mnemonic accumulator (Wagner, Shannon, Kahn, & Buckner, 2005), in directing internal attention (Cabeza, 2008; Cabeza et al., 2008, 2012), or as a gauge of memory subjectivity or confidence (Ally, Simons, McKeever, Peers, & Budson, 2008; Simons et al., 2008; Simons, Peers, Mazuz, Berryhill, & Olson, 2010). However, existing models linking spatial memory and episodic memory do not provide an integrated account to explain the performance of patients such as DM who presents bilateral hippocampal lesions and parietal atrophy and exhibit both spatial and episodic deficits. Instead, DM’s results support more specifically the egocentricupdating hypothesis (which postulates the presence of a memory of egocentric-updating in the BBB model) since it predicts both episodic and spatial memory disorders. This hypothesis suggests that episodic recollection occurs when the re-instantiation of a specific point of

view is processed fluently. Such a re-instantiation would involve cooperation between parietal and temporal areas (Gomez, Cerles, Rousset, Le Bas, & Baciu, 2013). This fluency is due to the initial egocentric-updating processing which occurred during encoding. Since patients suffering from hippocampal amnesia such as DM lack online egocentric-updating, and if fluency in the egocentricupdating process is responsible for the feeling of autonoetic consciousness (as suggested by previous results, i.e., Cerles & Rousset, 2012; Gomez et al., 2009), amnesia could be envisaged as a consequence of this online egocentric-updating deficit. During retrieval, amnesic patients would not be able to disentangle imaginary reconstruction (based on semantic memories) from real episodic ones as these episodic memories would lack both their spatial context and their autonoetic consciousness “tag”. To conclude, this case report provides for the first time a compelling behavioral dissociation among episodic memory components (what, where, when), as well as a striking co-occurrence of episodic and egocentric-updating spatial deficits in a case of developmental amnesia that must be taken into account by future episodic memory models. Acknowledgements We thank all participants, in particular Ms. DM, for their time and effort. The authors would also like to thank Elise Antoine, Mélanie Cerles, and Sophie Lemmonier for their precious experimental contribution.

Funding This work was partially funded by a French grant of the research and national education department.

Supplementary material Supplementary (Figure A/Figure B) is available via the “Supplementary” tab on the article’s online page (http://dx.doi. org/10.1080/13554794.2014.890730).

Notes 1.

2.

Surprisingly, this deficit spares the very recent period (last few months). On inquiry DM also appeared perfectly oriented in time and space. Both preservations appear to be at odds with what is generally observed in acquired amnesia following hippocampal lesions and were probably underpinned by compensatory strategies: in fact, helped by her entourage and relatives, DM uses rehearsal strategies for significant events of her recent life which might explain her performance. This reliance on compensatory strategies could have been favored by the developmental nature of her amnesia. To control for the encoding-test delay: (a) a Rotation trial was always tested before a no-rotation trial, (b) during each rotation trial, the experimenter recorded the encoding-test

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3.

delay, (c) this delay was then replicated in the following norotation trial. Data analysis: For each condition or subtest, modified t-tests (Crawford, Howell, & Garthwaite, 1998) were carried out to compare DM’s performance with that of the CG.When a classical functional dissociation was assessed between conditions, a modified Z-score was calculated following Crawford, Garthwaite, and Gray’s recommendations (Crawford, Garthwaite, & Howell, 2009). This score respect the three following criterion for two tasks X and Y: Criterion 1 – Patient’s score on task X is significantly lower than controls using Crawford et al. (1998) modified t-test method. Criterion 2 – Patient’s score on task Y is not significantly lower than in the control group (i.e., score fails to meet threshold for a deficit and is therefore considered to be within normal limits). Criterion 3 – Patient’s score on task X is significantly lower than patient’s score on task Y using Crawford et al. (1998) test.

4.

DM only reported two very unspecific spatial elements of the event (“one of the rooms was slightly bigger”, “I was standing”). Such elements were never included for control participants who always provided clear spatial elements such as: “the room was not larger than 15 m2”, “there was a window on the opposite side of the door”, “there was a bookshelf on the left”, “a chair on the right”… Excluding the two very unspecific spatial elements from the analysis does not qualitatively modify the results (T = −2.17, p = 0.0581).

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