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A comparison of egocentric and allocentric spatial memory in a patient with selective hippocampal damage
Abstract
The spatial memory of a single patient (YR) was investigated. This patient, who had relatively selective bilateral hippocampal damage, showed the pattern of impaired recall but preserved item recognition on standardised memory tests that has been suggested by Aggleton and Shaw [Aggleton JP, Shaw C. Amnesia and recognition memory: a reanalysis of psychometric data. Neuropsychologia 1996;34:51-62] to be a consequence of Papez circuit lesions. YR was tested on three recall tests and one recognition test for visuospatial information. The initial recall test assessed visuospatial memory over very short unfilled delays and YR was not significantly impaired. This test was then modified to test recall of allocentric and egocentric spatial information separately after filled delays of between 5 and 60 s. YR was found to be more impaired at recalling allocentric than egocentric information after a 60 s interval with a tendency for the impairment to increase up to this delay. Recognition of allocentric spatial information was also assessed after delays of 5 and 60 s. YR was impaired after the 60 s delay. The results suggest that the human hippocampus has a greater involvement in allocentric than egocentric spatial memory, and that this most likely concerns the consolidation of allocentric information into long-term memory rather than the initial encoding of allocentric spatial information. The findings also suggest that YR's item recognition/free recall deficit pattern reflects a problem retrieving or storing certain kinds of associative information.
... Indeed, sighted human patients with lesions to the parahippocampus are incapable of learning a new route (Hublet and Demeurisse, 1992;Maguire, 2001). In fact, a case study demonstrates that a lesion to the hippocampus has an effect mostly on the allocentric representation of a path (Holdstock et al., 2000). The parahippocampal area is also involved in the recognition of visual scenes used to navigate (Epstein and Kanwisher, 1998;Epstein et al., 2007). ...
... When participants try to solve a maze while in the scanner, the recorded activity is stronger in the right hippocampus (Maguire et al., 1997;Gagnon et al., 2012). Many studies have involved the hippocampus in topographic memory of places (Burgess et al., 2002) and allocentric representations (O'Keefe, 1991;Holdstock et al., 2000). A study demonstrated that the modulation of the interaction between the hippocampus and frontal or parietal regions depends on the type of strategy used in navigation (Mellet et al., 2000). ...
... Using fMRI, different activations for egocentric and allocentric navigations are also found, but with certain nuances (Shelton and Gabrieli, 2004). In a fMRI study, Holdstock et al. (2000) reported that the hippocampus is more activated by allocentric tasks, and confirmed previous data reported in humans and animals (O'Keefe, 1991). In this study, the authors show that a parietal network is involved in navigation in both conditions, but that the frontal region is only present in the egocentric condition. ...
In congenital blindness (CB), tactile, and auditory information can be reinterpreted by the brain to compensate for visual information through mechanisms of brain plasticity triggered by training. Visual deprivation does not cause a cognitive spatial deficit since blind people are able to acquire spatial knowledge about the environment. However, this spatial competence takes longer to achieve but is eventually reached through training-induced plasticity. Congenitally blind individuals can further improve their spatial skills with the extensive use of sensory substitution devices (SSDs), either visual-to-tactile or visual-to-auditory. Using a combination of functional and anatomical neuroimaging techniques, our recent work has demonstrated the impact of spatial training with both visual to tactile and visual to auditory SSDs on brain plasticity, cortical processing, and the achievement of certain forms of spatial competence. The comparison of performances between CB and sighted people using several different sensory substitution devices in perceptual and sensory-motor tasks uncovered the striking ability of the brain to rewire itself during perceptual learning and to interpret novel sensory information even during adulthood. We discuss here the implications of these findings for helping blind people in navigation tasks and to increase their accessibility to both real and virtual environments.
... In addition to the above, there is also a considerable collection of neuropsychological data indicating that the human hippocampus, as well as the parahippocampal gyrus, may have a significant role in spatial memory and navigation. Patients with hippocampal and/or parahippocampal damage are known to be significantly impaired in spatial memory and navigation (Bohbot, Iaria, & Petrides, 2004;Bohbot et al., 1998;Burgess, Maguire, & O'Keefe, 2002;Feigenbaum & Morris, 2004;Holdstock et al., 2000b;King, Burgess, Hartley, Vargha-Khadem, & O'Keefe, 2002;King, Trinkler, Hartley, Vargha-Khadem, & Burgess, 2004;Spiers, Burgess, Hartley, Vargha-Khadem, & O'Keefe, 2001b). Additionally, there is now evidence that there are cells within the human MTL, analogous to those found in the rat and monkey hippocampus, that signal aspects of space processing, with cells sensitive to location in the hippocampus and cells sensitive to views of landmarks in the parahippocampal gyrus (Ekstrom et al., 2003). ...
... The finding of deficits in both the HC and MTL groups in the scenes task further supports the idea that the human hippocampus may be critical to spatial perception and, furthermore, is consistent with the myriad of evidence demonstrating deficits in spatial memory following hippocampal damage (Bohbot et al., 2004;Bohbot et al., 1998;Burgess et al., 2002;Feigenbaum & Morris, 2004;King et al., 2002;King et al., 2004;Spiers et al., 2001b). Interestingly, recent studies have reported impaired allocentric, but not egocentric, memory for spatial scenes in patients with selective hippocampal lesions (Bohbot et al., 2004;Feigenbaum & Morris, 2004;Holdstock et al., 2000b;King et al., 2002;King et al., 2004). In general, patients with hippocampal damage are comparable to healthy control subjects or only mildly impaired at recognizing object locations that are viewed from the same viewpoint as that during the learning phase (i.e., intact egocentric memory). ...
The medial temporal lobe (MTL) has been considered traditionally to subserve declarative memory processes only. Recent studies in nonhuman primates suggest, however, that the MTL may also be critical to higher order perceptual processes, with the hippocampus and perirhinal cortex being involved in scene and object perception, respectively. The current article reviews the human neuropsychological literature to determine whether there is any evidence to suggest that these same views may apply to the human MTL. Although the majority of existing studies report intact perception following MTL damage in human amnesics, there have been recent studies that suggest that when scene and object perception are assessed systematically, significant impairments in perception become apparent. These findings have important implications for current mnemonic theories of human MTL function and our understanding of human amnesia as a result of MTL lesions.
... The dichotomy in spatial reference frame is also supported in the neuroscience research. For example, there exists different neural structures and visual processing pathways for egocentric and allocentric RFs (Galati, Lobel, Vallar, Berthoz, Pizzamiglio, andLe Bihan, 2000 andHoldstock, Mayes, Cezayirli, Isaac, Aggleton, andRoberts, 2000). ...
... The dichotomy in spatial reference frame is also supported in the neuroscience research. For example, there exists different neural structures and visual processing pathways for egocentric and allocentric RFs (Galati, Lobel, Vallar, Berthoz, Pizzamiglio, andLe Bihan, 2000 andHoldstock, Mayes, Cezayirli, Isaac, Aggleton, andRoberts, 2000). ...
Spatial reference frames (SRF) are the means of representing spatial relations or locations either in an egocentric coordinate system (centred on navigator) or in an allocentric coordinate system (Centred on object). It is necessary to understand when and how spatial representation switches between allocentric and egocentric reference frames in context to spatial tasks. The objective of this study was to explore if the elementary spatial representation does exist, whether it would remain consistent or change under the influence of a task's demand. Also, we explored how the SRF would assist if the environment is enriched with landmarks, having multiple routes for wayfinding. The results showed that the switching of SRF depends not only on the default representation but also on a task's demand. They also demonstrated that participants who were using allocentric representation performed better in the presence of landmarks.
... SpeciWcally, neurons in the monkey lateral intraparietal area-an area thought to be homologous to the human angular gyrus-respond to the egocentric distance between an object and a body part, such as the monkey's hand (Genovesio and Ferraina 2004;Sakata et al. 1997). In contrast, damage to the ventral visual stream extending into the medial temporal lobe, causes disproportionate deWcits in allocentric spatial memory Hartley et al. 2007;Holdstock et al. 1999Holdstock et al. , 2000Murphy et al. 1998; but see Shrager et al. 2007). The well-known patient DF, who has bilateral ventral stream lesions, exhibits intact egocentric task performance, but impaired performance when forced to apply an allocentric reference frame Carey et al. 2006;Murphy et al. 1998). ...
... EE555's preserved abilities to utilize familiar size information, her probable use of accommodation and vergence, and her ability to compute allocentric distance indicate that these functions rely on neural processing mechanisms that are distinct from those needed to compute distance based on binocular and most monocular pictorial cues. Ventral stream regions intact in EE555 are thought to compute familiar size (e.g., Marotta and Goodale 2001) and allocentric distance perception Hartley et al. 2007;Holdstock et al. 1999Holdstock et al. , 2000Murphy et al. 1998). One fMRI study has linked a small midline occipitoparietal region to convergence and accommodation (Quinlan and Culham 2007), a neural region that is also preserved in Patient EE555. ...
Accurate distance perception depends on the processing and integration of a variety of monocular and binocular cues. Dorsal stream lesions can impair this process, but details of this neurocognitive relationship remain unclear. Here, we tested a patient with bilateral occipitoparietal damage and severely impaired stereopsis. We addressed four related questions: (1) Can distance and size perception survive limitations in perceiving monocular and binocular cues? (2) Are egocentric (self-referential) and allocentric (object-referential) distance judgments similarly impaired? (3) Are distance measurements equally impaired in peripersonal and extrapersonal space? (4) Are size judgments possible when distance processing is impaired? The results demonstrate that the patient's lesions impaired both her distance and size perception , but not uniformly. Her performance when using an egocentric reference frame was more impaired than her performance when using an allocentric reference frame. Likewise , her distance judgments in peripersonal space were more impaired than those in extrapersonal space. The patient showed partial preservation in size processing of novel objects even when familiar size cues were removed.
... In the current study, there were no group differences across types of selfreported strategies; however, other reports suggest reduced use of ALLO representations in SCZ (Hanlon et al., 2006;Manoach et al., 2005). In addition, the current SCZ group was impaired on the mental rotation task, whereas mental rotation has not previously been associated with performance on the bin task (Abrahams et al., 1997;Rahman et al., 2005) or hippocampal dysfunction (Abrahams et al., 1997;Holdstock et al., 2000;J. A. King, Burgess, Hartley, Vargha-Khadem, & O'Keefe, 2002). ...
Objective: Enhanced understanding of cognitive deficits, and the neurobiological abnormalities that mediate them, can be achieved through translational research that employs comparable experimental approaches across species. This study employed a multiple-systems framework derived from the rodent literature to investigate visual–spatial memory abilities associated with schizophrenia. Method: Using the bin task, a human analog of rodent maze tasks, everyday objects were hidden in visually identical bins. Following a 1-min filled delay, participants with schizophrenia-spectrum disorders (n = 30) and healthy community controls (n = 30) were asked to identify both the object hidden and bin used on the basis of its spatial location. Three dimensions of visual–spatial memory were contrasted: (a) memory for spatial locations versus memory for objects, (b) allocentric (viewpoint independent) versus egocentric (body-centered) spatial representations, and (c) event (working) memory versus reference memory. Results: Most pronounced was a differential deficit in memory for spatial locations under allocentric (p = .005, d = −0.77) but not egocentric viewing conditions (p = .298, d = −0.28) in the schizophrenia group relative to healthy controls. Similarly, schizophrenia-related spatial memory deficits were pronounced under demands for event memory (p = .004, d = −0.77) but not reference memory (p = .171, d = −0.33). Conclusions: These results support a heuristic of preferential deficits in hippocampal-mediated forms of memory in schizophrenia. Moreover, the task provides a useful paradigm for translational research and the pattern of deficits suggests that persons with schizophrenia may benefit from mnemonic approaches favoring egocentric representations and consistency when interacting with our visual–spatial world.
... All rights reserved. consolidation of allocentric information in long-term memory [13,14]. The Morris water navigation maze and the Barnes maze, often referred to as the dry equivalent of the Morris water maze, are considered most appropriate for this task [15][16][17]. ...
Temporal lobe epilepsy (TLE) often causes cognitive impairment, especially a decline in spatial memory. Reductions in spatial memory and learning are also common in rodent models of TLE. The Morris water maze and the Barnes maze are the standard methods for evaluating spatial learning and memory in rodents. However, animals with TLE may exhibit agitation, distress, and fail to follow the paradigmatic context of these tests, making the interpretation of experimental data difficult. This study optimized the procedure of the Morris water maze and the Barnes maze to evaluate spatial learning and memory in rats with the lithium-pilocarpine TLE model (LPM rats). It was demonstrated that LPM rats required a mandatory and prolonged habituation stage for both tests. Therefore, the experimental rats performed relatively well on these tests. Nevertheless, LPM rats exhibited a slower learning process compared to the control rats. LPM rats also showed a reduction in spatial memory formation. This was more pronounced in the Barnes maze. Also, LPM rats utilized a sequential strategy for searching in the Barnes maze and were incapable of developing a more efficient spatial search strategy that is common in control animals. The Barnes maze may be a better choice for assessing search strategies, learning deficits, and spatial memory in rats with TLE when choosing between the two tests. This is because of the risk of unexpected seizure occurrence during the Morris water maze tests, and the potential risks for animal welfare.
... ; https://doi.org/10.1101/2023.03.23.533994 doi: bioRxiv preprint hippocampal clustering using a spatial learning experiment. Spatial navigation was selected due to its long-standing connection with hippocampus when navigating in novel environments (11)(12)(13)(14)(15)(16)(17)(18) plus its waning influence during navigation of well-learned environments (16,(19)(20)(21)(22)(23). In our experiment, subjects were trained to virtually navigate a novel neighborhood in a Google Street View-like environment ( Figures 1A, 1C-1E) over a two-week period (7 sessions). ...
Structural differences along the long-axis of the hippocampus have long been believed to underlie meaningful functional differences, such as the granularity of information processing. Recent findings show that data-driven parcellations of the hippocampus sub-divide the hippocampus into a 10-cluster map with anterior-medial, anterior-lateral, and posteroanterior-lateral, middle, and posterior components. We tested whether task and experience could modulate this clustering using a spatial learning experiment where subjects were trained to virtually navigate a novel neighborhood in a Google Street View-like environment over a two-week period. Subjects were scanned while navigating routes early in training and at the end of their two-week training. Using the 10-cluster map as the ideal template, we find that subjects who eventually learn the neighborhood well have hippocampal cluster-maps consistent with the ideal--even on their second day of learning--and their cluster mappings do not change over the two week training period. However, subjects who eventually learn the neighborhood poorly begin with hippocampal cluster-maps inconsistent with the ideal, though their cluster mappings become more stereotypical by the end of the two week training. Interestingly this improvement seems to be route specific as even after some early improvement, when a new route is navigated participants' hippocampal maps revert back to less stereotypical organization. We conclude that hippocampal clustering is not dependent solely on anatomical structure, and instead is driven by a combination of anatomy, task, and importantly, experience. Nonetheless, while hippocampal clustering can change with experience, efficient navigation depends on functional hippocampal activity clustering in a stereotypical manner, highlighting optimal divisions of processing along the hippocampal anterior-posterior and medial-lateral-axes.
... In contrast, body-referencing, or egocentric representation is constructed of spatial relations between the body and objects which leads to a spatial representation that is dependent upon the point of view (Burgess, 2006). Allocentric spatial representation is thought to rely mainly on the hippocampus (Galati et al., 2010;Hartley et al., 2007;Holdstock et al., 2000;Morris et al., 1982;Parslow et al., 2004;Spiers, Burgess, Maguire, et al., 2001). ...
Inuit communities in Northern Quebec (Canada) are exposed to environmental contaminants, particularly to mercury, lead and polychlorinated biphenyls (PCBs). Previous studies reported adverse associations between these neurotoxicants and memory performance. Here we aimed to determine the associations of pre- and postnatal exposures to mercury, lead and PCB-153 on spatial navigation memory in 212 Inuit adolescents (mean age = 18.5 years) using a computer task which requires learning the location of a hidden platform based on allocentric spatial representation. Contaminant concentrations were measured in cord blood at birth and blood samples at 11 years of age and at time of testing. Multivariate regression models showed that adolescent mercury and prenatal PCB-153 exposures were associated with poorer spatial learning, whereas current exposure to PCB-153 was associated with altered spatial memory retrieval at the probe test trial. These findings suggest that contaminants might be linked to different aspects of spatial navigation processing at different stages.
... Nunn et al. (1999) found dissociations in patients with righttemporal lobectomy, showing that their memory for the location of objects was worse than memory for the objects themselves, despite controlling for the problem of differential sensitivities of the tasks to overall memory impairment. At an individual level, Holdstock et al. (2000) reported on the case of a patient (YR) with relatively selective bilateral hippocampal damage who was impaired on tasks related to spatial memory but exhibited intact visual recognition on standardized memory tests. Additionally, Kessels et al. (2002) showed that there was a double dissociation between patients with left hemisphere strokes (showing impairment on object location binding) and right hemisphere strokes (impaired on positional memory and maze learning), and a specific impairment for spatialmemory tasks in those patients with lesions in the posterior part of the parietal or the occipital lobe; thus showing evidence for selective aspects of memory for object locations. ...
A proliferation of tests exists for the assessment of auditory-verbal memory processes. However, from a clinical practice perspective, the situation is less clear when it comes to the ready availability of reliable and valid tests for the evaluation of visual/visuo-spatial memory processes. While, at face value, there appear to be a wide range of available tests of visual/visuo-spatial memory, utilizing different types of materials and assessment strategies, a number of criticisms have been, and arguably should be, leveled at the majority of these tests. The criticisms that have been directed toward what are typically considered to be visual/visuo-spatial memory tests, such as (1) the potential for verbal mediation, (2) over-abstraction of stimuli, (3) the requirement of a drawing response, and (4) the lack of sensitivity to unilateral brain lesions, mean that, in reality, the number of readily available valid tests of visual/visuo-spatial memory is, at best, limited. This article offers a critical, historical review on the existing measures and resources for the neuropsychological assessment of visual/visuo-spatial memory, and it showcases some examples of newer tests that have aimed to overcome the challenges of assessing these important aspects of memory. The article also identifies new trends and examples of how technological advances such as virtual reality may add value to overcome previous obstacles to assessment, thereby offering professionals more reliable, accurate means to evaluate visual/visuo-spatial memory in clinical practice.
... The cognitive map theory proposes that the hippocampus stores information in maps that are allocentric or independent of the observer's personal perspective, which helps individuals to locate places in their environments (O'Keefe & Nadel, 1978). This theory has been corroborated in human studies (Feigenbaum & Morris, 2004;Holdstock et al., 2000;Kessels et al., 2001;Parslow et al., 2004), but a case study of a patient with traumatic brain injury-induced amnesia showed that the hippocampus is not critical for landmark representation during spatial navigation (Kolarik et al., 2016). With the aim of integrating knowledge about visual memory in other forms of perceptual processing, the binding theory holds that the hippocampus acts as an integrative structure that binds information on items and location/context into events (Chalfonte et al., 1996). ...
Introduction:
The Ruche test is a visuospatial form of the Rey auditory verbal learning test (RAVLT), with initial evidence of utility in the diagnosis of temporal lobe epilepsy (TLE)-related memory disorders.
Aims:
To present the translation to Brazilian Portuguese and modification of the Ruche test (RUCHE-M) and compare the RUCHE-M and RAVLT performance between patients with right and left TLE.
Methods:
Twenty-five neuropsychologists participated in instrument adaptation. Thirty-seven patients with right (n = 19) and left (n = 18) TLE participated. Data were compared with the Mann-Whitney U test.
Results:
All specialists considered the final RUCHE-M to be adequate. The RUCHE-M forgetting speed index (FSI) score and several RAVLT scores differed significantly between patients with right and left TLE.
Conclusion:
The RUCHE-M showed limited utility for the assessment of visuospatial episodic memory in patients with TLE. The manipulation of memory binding as demonstrated by FSI score seems to be a promising paradigm for the assessment of right hippocampal function.
... Neuroimaging studies have found hippocampal volume reduction in schizophrenia patients (Wright et al., 2000). This is particularly relevant since the hippocampus plays a central role in spatial memory, navigation, and in particular in allocentric spatial information (Burgess, Maguire, & O'Keefe, 2002;Holdstock et al., 2000;Iaria, Petrides, Dagher, Pike, & Bohbot, 2003). In addition, there is cumulating evidence that the hippocampus plays a key role in the transformation from egocentric to allocentric representations (Wang, Chen, & Knierim, 2020), which may explain why schizophrenia patients had difficulty with both the viewer and object rotation tasks, which are in allocentric and egocentric reference frames, respectively. ...
Schizophrenia patients have difficulty with processing visuo-spatial information, which may explain their deficits with considering other people's point-of-view. Processing visuo-spatial information operates on egocentric and allocentric frames of reference. Here, we tested the ability of individuals at different stages of psychotic disorders, specifically ultra-high-risk for psychosis individuals, as well as first-episode psychosis, and chronic schizophrenia patients, to perform a viewer mental rotation task and an object mental rotation task. The two tasks were differentiated only by the instruction given. Healthy individuals and patients with a diagnosis of anxiety/depressive mood disorder served as non-patient and patient controls, respectively. The results show that first-episode psychosis and chronic schizophrenia patients, but not ultra-high-risk individuals, had more errors and longer response times with both mental rotation tasks than the two control groups. In addition, chronic schizophrenia patients had additional difficulty with the object rotation task. The difference in performance between groups and tasks remained significant even after controlling for age, IQ, and antipsychotic medication dose. The results indicate that patients with psychotic disorders have a deficit of mental spatial imagery that include both egocentric and allocentric representations. This deficit may explain the difficulty of these patients with perspective-taking, and inferring other people's point of view, thoughts or intentions which is at the core of the pathogenesis of schizophrenia.
... Damage to the hippocampus often results in spatial memory problems (Astur et al., 2002;Holdstock et al., 2000). The right hippocampus is particularly important for spatial memories (Brown et al., 2016;O'keefe & Nadel, 1978). ...
Human spatial memories are usually evaluated using computer screens instead of real arenas or landscapes where subjects could move voluntarily and use allocentric cues to guide their behavior. A possible approach to fill this gap is the adoption of virtual reality, which provides the opportunity to create spatial memory tasks closer to real-life experience. Here we present and evaluate a new software to create experiments using this technology. Specifically, we have developed a spatial memory task that is carried out in a computer-assisted virtual environment where participants walk around a virtual arena using a joystick. This spatial memory task provides an immersive environment where the spatial component is constantly present without the use of virtual reality goggles. The design is similar to that of tasks used for animal studies, allowing a direct comparison across species. We found that only participants who reported using spatial cues to guide their behavior showed significant learning and performed significantly better during a memory test. This tool allows evaluation of human spatial memory in an ecological environment and will be useful to develop a wide range of other tasks to assess spatial cognition.
... For example, patients with parietal lobe lesions exhibit deficits on egocentric tests of spatial cognition such as landmark sequencing and route navigation, but are unimpaired on allocentric spatial tasks that involve imagining a map of landmark locations (Ciaramelli et al. 2010;Weniger et al. 2009). In contrast, patients with hippocampal lesions have been found to be impaired on tasks assessing allocentric but not egocentric spatial memory (Holdstock et al. 2000;Rosenbaum et al. 2000). ...
The ability to remember events in vivid, multisensory detail is a significant part of human experience, allowing us to relive previous encounters and providing us with the store of memories that shape our identity. Recent research has sought to understand the subjective experience of remembering, that is, what it feels like to have a memory. Such remembering involves reactivating sensory-perceptual features of an event and the thoughts and feelings we had when the event occurred, integrating them into a conscious first-person experience. It allows us to reflect on the content of our memories and to understand and make judgments about them, such as distinguishing events that actually occurred from those we might have imagined or been told about. In this review, we consider recent evidence from functional neuroimaging in healthy participants and studies of neurological and psychiatric conditions, which is shedding new light on how we subjectively experience remembering.
Expected final online publication date for the Annual Review of Psychology, Volume 73 is January 2022. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
... According to Holdstock et al. (2000), declarative spatial memory can be subdivided into allocentric spatial memory (memory of the position of objects or stimuli, which is independent of the observer) and egocentric spatial memory (which is related to the observer). Specifically, the hippocampus is involved through the allocentric and dorsolateral striatum in the egocentric spatial memory (Sarkisyan and Hedlund, 2009). ...
Cognitive dysfunction is one of the most severe nonmotor symptoms of nigrostriatal impairment. This occurs as a result of profound functional and morphological changes of different neuronal circuits, including modifications in the plasticity and architecture of hippocampal synapses. Such alterations can be implicated in the genesis and progression of dementia associated with neurodegenerative diseases including Parkinson-like symptoms. There are few studies regarding cognitive changes in nigrostriatal animal models. The aim of this study was to characterize the onset of memory deficit after induction of neurotoxicity with 6-hydroxydopamine (6-OHDA) and its correlation with hippocampal dysfunction. For this, we bilaterally microinjected 6-OHDA in dorsolateral Caudate-Putamen unit (CPu) and then, animals were tested weekly for working memory, spatial short-term memory, and motor performance. We evaluated tyrosine hydroxylase (TH) as a dopamine marker, aldehyde dehydrogenase 2 (ALDH2), a mitochondria detoxification enzyme and astrocyte glial fibrillar acid protein (GFAP) an immunoreactivity marker involved in different areas: CPu, substantia nigra, prefrontal cortex, and hippocampus. We observed a specific prefrontal cortex and nigrostriatal pathway TH reduction while ALDH2 showed a decrease-positive area in all the studied regions. Moreover, GFAP showed a specific CPu decrease and hippocampus increase of positively stained area on the third week after toxicity. We also evaluated the threshold to induce long-term potentiation in hippocampal excitability. Our findings showed that reduced hippocampal synaptic transmission was accompanied by deficits in memory processes, without affecting motor performance on the third-week post 6-OHDA administration. Our results suggest that 3 weeks after neurotoxic administration, astrocytes and ALDH2 mitochondrial enzyme modifications participate in altering the properties that negatively affect hippocampal function and consequently cognitive behavior.
... Concerning the underlying neural correlates, the hippocampus is crucial in using allocentric frames of reference (e.g., O'Keefe and Nadel, 1978;Maguire et al., 1998;Holdstock et al., 2000). Although KS is primarily characterized by diencephalic lesions (Aggleton and Saunders, 1997;Arts et al., 2017), hippocampal atrophy has been reported in these patients as well (e.g., Sullivan and Pfefferbaum, 2009). ...
The goal of the present study was to investigate spatial memory in a group of patients with amnesia due to Korsakoff’s syndrome (KS). We used a virtual spatial memory task that allowed us to separate the use of egocentric and allocentric spatial reference frames to determine object locations. Research investigating the ability of patients with Korsakoff’s amnesia to use different reference frames is scarce and it remains unclear whether these patients are impaired in using ego- and allocentric reference frames to the same extent. Twenty Korsakoff patients and 24 matched controls watched an animation of a bird flying in one of three trees standing in a virtual environment. After the bird disappeared, the camera turned around, by which the trees were briefly out of sight and then turned back to the center of the environment. Participants were asked in which tree the bird was hiding. In half of the trials, a landmark was shown. Half of the trials required an immediate response whereas in the other half a delay of 10 s was present. Patients performed significantly worse than controls. For all participants trials with a landmark were easier than without a landmark and trials without a delay were easier than with a delay. While controls were above chance on all trials patients were at chance in allocentric trials without a landmark present and with a memory delay. Patients showed no difference in the ego- and the allocentric condition. Together the findings suggest that despite the amnesia, spatial memory and especially the use of ego- and allocentric reference frames in Korsakoff patients are spared.
... Forming a cognitive map of the environment, as is accomplished in allocentric processing, requires the integration of landmarks in the environment and depends on hippocampal function (O'Keefe and Nadel, 1978;Bohbot et al., 2004;Nadel and Hardt, 2004;Chersi and Burgess, 2015). Imaging studies have revealed that allocentric information processing is associated with elevated hippocampal activity (Bohbot et al., 2004;Parslow et al., 2005;Zaehle et al., 2007) and patients with hippocampal damage show impaired performance on tasks that require allocentric processing (Holdstock et al., 2000;Bohbot et al., 2004;Feigenbaum and Morris, 2004). ...
An important aspect concerning the underlying nature of memory function is an understanding of how memories are acquired and lost. The stability, and ultimate demise, of memory over the lifespan of an organism remains a critical topic in determining the neurobiological mechanisms that mediate memory representations. This has important implications for the elucidation and treatment of neurodegenerative diseases such as Alzheimer’s disease (AD). One important question in the context of preserving functional plasticity over the lifespan is the determination of the neurobiological structural and functional changes that contribute to the formation of memory during the juvenile time frame that might provide protection against later memory dysfunction by promoting the establishment of redundant neural pathways. The main question being, if memory formation during the juvenile period does strengthen and preserve memory stability over the lifespan, what are the neurobiological structural or functional substrates that mediate this effect? One neural attribute whose function may be altered with early life experience and provide a mechanism to preserve memory through the lifespan is glucose transport-linked calcium (Ca2+) buffering. Because peak increases in glucose utilization overlap with a timeframe during which spatial training can enhance later memory processing, it might be the case that learning-associated changes in glucose utilization would provide an important neural functional change to preserve memory function throughout the lifespan. The glucose transporters are proteins that are reduced in AD pathology and there is evidence that glucose reductions can impair Ca2+ buffering. In the absence of an appropriate supply of ATP, provided via glucose transport and glycolysis, Ca2+ levels can rise leading to neural vulnerability with ensuing pathological outcomes. In this review, we explore the hypothesis that enhancing glucose utilization with spatial training during the preadolescent period will provide a functional enhancement that regulates glucose-dependent Ca2+ signaling during aging or neurodegeneration and provide essential neural resources to preserve functional plasticity and memory function.
... Indeed, neuroimaging studies looking for correlates of allocentric coding have frequently identified higher areas in the ventral stream [68][69][70][71][72][73] as components of a broader distributed network contributing to allocentric representation [65,71]. Hippocampal structures are also implicated in relative spatial encoding, most clearly in relation to navigation, but with growing evidence for a role in coding visual space [59,71,[74][75][76][77][78]. ...
Visuospatial working memory enables us to maintain access to visual information for processing even when a stimulus is no longer present, due to occlusion, our own movements, or transience of the stimulus. Here we show that, when localizing remembered stimuli, the precision of spatial recall does not rely solely on memory for individual stimuli, but additionally depends on the relative distances between stimuli and visual landmarks in the surroundings. Across three separate experiments, we consistently observed a spatially selective improvement in the precision of recall for items located near a persistent landmark. While the results did not require that the landmark be visible throughout the memory delay period, it was essential that it was visible both during encoding and response. We present a simple model that can accurately capture human performance by considering relative (allocentric) spatial information as an independent localization estimate which degrades with distance and is optimally integrated with egocentric spatial information. Critically, allocentric information was encoded without cost to egocentric estimation, demonstrating independent storage of the two sources of information. Finally, when egocentric and allocentric estimates were put in conflict, the model successfully predicted the resulting localization errors. We suggest that the relative distance between stimuli represents an additional, independent spatial cue for memory recall. This cue information is likely to be critical for spatial localization in natural settings which contain an abundance of visual landmarks.
... Lesion studies in humans and animals (Ekstrom et al., 2003;Maguire et al., 1997;O'Keefe and Nadel, 1979;Rolls, 1999;Rolls and Xiang, 2006) and functional imaging studies in humans (Aguirre et al., 1996;Aguirre and D'Esposito, 1997;Barry et al., 2006;Bohbot et al., 2007Bohbot et al., , 2004Burgess et al., 2001;Epstein et al., 2003;Etchamendy et al.,2012;Holdstock et al., 2000;Iaria et al., 2003;King et al., 2002;Maguire et al., 1997;Siemerkus et al., 2012) have suggested that allocentric navigation is dependent upon the hippocampal and parahippocampal cortices. Weinberger's group showed that an abnormal cortical response was observed in the DLPFC of patients with schizophrenia while performing spatial working memory tasks. ...
Dysfunction of allocentric and egocentric memories is one of the core features of psychiatric disorders. There are a few navigational studies on these memories in schizophrenia and bipolar disorders, but studies in schizoaffective disorder are lacking. Here, we aim to explore allocentric and egocentric navigation deficits in these subjects using our advanced recently developed virtual reality navigation task (VRNT). Twenty patients with schizophrenia and 20 with schizoaffective disorder were compared with 20 normal volunteer subjects on VRNTs consisting of a virtual neighbourhood (allocentric memory) and a virtual maze (egocentric memory). Compared with schizoaffective disorder and control subjects, patients with schizophrenia had the worst performance on both virtual neighbourhood and virtual maze tasks. The allocentric memory in both patients with schizophrenia and those with schizoaffective disorder was more impaired than the egocentric memory (p˂0.001). However, the patients with schizoaffective disorder performed better in egocentric memory than those with schizophrenia, as they had fewer errors in the virtual maze. It was concluded that allocentric memory is more impaired than egocentric in both schizoaffective disorder and schizophrenia patients, whereas patients with schizoaffective disorder performed better in egocentric memory than patients with schizophrenia. It was also concluded that allocentric memory deficits can help differentiate patients with schizophrenia and schizoaffective disorder from healthy participants, whereas egocentric memory deficits can be used to distinguish them from each other.
... It is generally accepted that the hippocampus plays a key role in spatial memory (Holdstock et al., 2000). However, the extent of its involvement and the interplay with extra-hippocampal areas seem to depend upon the specific context. ...
Objective: In subjects with mild cognitive impairment (MCI), interference during memory consolidation may further degrade subsequent recall of newly learned information. We investigated whether spatial and object memory are differentially susceptible to interference.
Method: Thirty-nine healthy young subjects, 39 healthy older subjects, and 12 subjects suffering from MCI encoded objects and their spatial position on a 4-by-5 grid. Encoding was followed by either: (i) a pause; (ii) an interference task immediately following encoding; or (iii) an interference task following encoding after a 6-min delay. Type of interference (no, early, delayed) was applied in different sessions and order was counterbalanced. Twelve minutes after encoding, subjects saw objects previously presented or new ones. Subjects indicated whether they recognized the object, and if so, the objects’ position during encoding.
Results: Interference during consolidation provoked a negative effect on spatial memory in young more than older controls. In MCI, object but not spatial memory was affected by interference. Furthermore, a shift from fine- to coarse-grained spatial representation was observed in MCI. No differential effect of early vs. late interference (EI vs. LI) in either of the groups was detected.
Conclusions: Data show that consolidation in healthy aging and MCI differs from consolidation in young controls. Data suggest differential processes underlying object and spatial memory and that these are differentially affected by aging and MCI.
... One prominent theory is that the hippocampus is critical for allocentric (landmark-guided) but not egocentric (self-oriented) spatial memory, and that navigation primarily taxes allocentric coding (e.g., Holdstock et al., 2000;Lavenex & Lavenex, 2009;Packard & McGaugh, 1996). In nonhuman primates, there is good but sparse evidence that the hippocampus is necessary for navigational tasks (Glavis-Bloom et al., 2013;Hampton, Hampstead, et al., 2004;Lavenex et al., 2006). ...
... Tasks requiring either spatial memory or navigation based on allocentric cues generally engage the hippocampus (Hartley, Maguire, Spiers, & Burgess, 2003;Iaria, Petrides, Dagher, Pike, & Bohbot, 2003;Kumaran & Maguire, 2005;Maguire et al., 1998) and are impaired in patients with hippocampal brain damage (Corkin, Amaral, González, Johnson, & Hyman, 1997;Feigenbaum & Morris, 2004;Guderian et al., 2015;Hartley et al., 2007;Holdstock et al., 2000;Scoville & Milner, 1957). Spatial navigation becomes gradually impaired during ageing. ...
Spatial learning, including encoding and retrieval of spatial memories as well as holding spatial information in working memory generally serving navigation under a broad range of circumstances, relies on a network of structures. While central to this network are medial temporal lobe structures with a widely appreciated crucial function of the hippocampus, neocortical areas such as the posterior parietal cortex and the retrosplenial cortex also play essential roles. Since the hippocampus receives its main subcortical input from the medial septum of the basal forebrain cholinergic system, it is not surprising that the potential role of the septo‐hippocampal pathway in spatial navigation has been investigated in many studies. Much less is known of the involvement in spatial cognition of the parallel projection system linking the posterior basal forebrain with neocortical areas. Here we review the current state of the art of the division of labour within this complex ‘navigation system’, with special focus on how subcortical cholinergic inputs may regulate various aspects of spatial learning, memory and navigation.
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... Most lesion studies support the idea that the MTL (in particular the right hemisphere) is critical for place learning (Abrahams et al. 1997;Holdstock et al. 1999Holdstock et al. , 2000 and goaldirected navigation (Astur et al. 2002;Maguire et al. 2006a;Spiers et al. 2001). In general, damage to this region impairs spatial memory but not object memory (Abrahams et al. 1997;Spiers et al. 2001). ...
Cognitive neuroscience can provide novel and interesting techniques for investigating spatial and geographic thinking. However, the incorporation of neuroscientific methods still lacks the theoretical motivation necessary for the progression of geography as a discipline. Rather than reflecting a shortcoming of neuroscience, this weakness has developed from previous attempts to establish a positivist approach to behavioral geography. In this chapter, we will discuss the challenges of establishing a positivist approach in behavioral geography and the current drive to incorporate neuroscientific evidence. Towards this end, we review research in geography and neuroscience. Here, we focus specifically on navigation and large-scale spatial thinking. We argue that research at the intersection of geography and neuroscience would benefit from an explanatory, theory-driven approach rather than a descriptive, exploratory approach. Future collaborations will require additional training for geographers and neuroscientists and the involvement of both disciplines during the early stages of a research program.
... The hippocampus is involved in long-term egocentric spatial memory, but short-term egocentric spatial memory largely depends on different cortical regions ( Moscovitch et al., 2005;Weniger, Ruhleder, Wolf, Lange & Irle, 2009). For ASM, however, the hippocampus is the crucial cortical structure for both long-term and short-term recollections ( Burgess, Maguire & O'Keefe, 2002;Byrne, Becker & Burgess, 2007;Holdstock et al., 2000;Yee, Hannula, Tranel & Cohen, 2014). Early literature on spatial memory and the hippocampus came from animal studies, including the identification of the hippocampus creating a cognitive map of the environment through the firing of "place cells" that respond to different features of the external surroundings (O' Keefe & Nadel, 1978). ...
Depression is associated with deficits in the recollection of specific autobiographical memories, a phenomenon referred to as overgeneral memory. Neither the modifiability nor the neural correlates of overgeneral memory are currently well understood. The aim of this thesis was to increase the understanding of autobiographical memory specificity and overgeneral memory in depression. Part one of the thesis is a literature review investigating whether interventions for treating and preventing depression are effective in improving autobiographical memory specificity. Nineteen studies of varying methodological strength were identified and included in the review. There is evidence that memory specificity improves over the course of treatment for depression, but further research is required to establish the causal effects of different interventions and the effectiveness of prevention strategies. Part two of the thesis presents an empirical study aimed at establishing the association between overgeneral memory and allocentric spatial memory as a measure of hippocampal function in depression. Depressed and non-depressed adults completed measures of autobiographical memory and allocentric spatial memory. The depression group showed impairment in autobiographical memory, but not in allocentric spatial memory, and there was no association between performance on the two memory tasks. The data was collected in the context of a joint project (Williams, 2017). Part three of the thesis is a critical appraisal of the research. It offers reflections on study design and recruitment, benefits of a joint project, exclusion criteria and generalizability, challenges in measuring autobiographical memory, and the role of a clinical researcher in the National Health Service.
... This reinforces the idea that the deficits observed in our patients are unlikely to be due to a fundamental deficit in mental rotation. Rather, it appears that patients with hippocampal damage may be unable to use viewpoint independent representations of spatial scenes, often referred to as allocentric representations (e.g., see Aguirre and D'Esposito, 1999;Holdstock et al., 2000b;Burgess et al., 2001;Bohbot et al., 2004;Feigenbaum and Morris, 2004;King et al., 2004). ...
There has been considerable debate as to whether the hippocampus and perirhinal cortex may subserve both memory and perception. We administered a series of oddity tasks, in which subjects selected the odd stimulus from a visual array, to amnesic patients with either selective hippocampal damage (HC group) or more extensive medial temporal damage, including the perirhinal cortex (MTL group). All patients performed normally when the stimuli could be discriminated using simple visual features, even if faces or complex virtual reality scenes were presented. Both patient groups were, however, severely impaired at scene discrimination when a significant demand was placed on processing spatial information across viewpoint independent representations , while only the MTL group showed a significant deficit in oddity judgments of faces and objects when object viewpoint independent perception was emphasized. These observations provide compelling evidence that the human hippocampus and perirhinal cortex are critical to processes beyond long-term declarative memory and may subserve spatial and object perception, respectively. V V C 2005 Wiley-Liss, Inc.
... Clinical studies can also address whether recollection and familiarity are supported by anatomically separate neural systems. Although most amnesic patients are impaired on both forms of memory, some patients that have selective damage to the hippocampus or connecting structures such as the fornix show impaired recollection with relatively preserved familiarity-based memory [31][32][33][34] . Again, other researchers have reported familiarity deficits after selective hippocampal damage 35 (FIG. ...
... Parietal patients were unimpaired on spatial tasks that were considered to rely on an allocentric strategy, such as imagining a map on which the various landmarks were located. This pattern contrasts with evidence from patients with selective hippocampal lesions, who are impaired on tasks assessing allocentric but not egocentric spatial memory [30]. Consistent with the notion of impairment in egocentric aspects of memory following parietal lobe damage, Berryhill et al. [31] observed that when patients with parietal lesions recalled past autobiographical events or imagined novel constructed experiences, they were less likely to represent themselves in the scenes that they created, reporting fewer details about their thinking, their emotional states and their own actions during their narratives. ...
Background: Lesions of the angular gyrus (AnG) region of human parietal cortex do not cause amnesia,
but appear to be associated with reduction in the ability to consciously experience the reliving of previous
events.
Objectives/Hypothesis: We used continuous theta burst stimulation to test the hypothesis that the
cognitive mechanism implicated in this memory deficit might be the integration of retrieved sensory
event features into a coherent multimodal memory representation.
Methods: Healthy volunteers received stimulation to AnG or a vertex control site after studying stimuli
that each comprised a visual object embedded in a scene, with the name of the object presented auditorily.
Participants were then asked to make memory judgments about the studied stimuli that
involved recollection of single event features (visual or auditory), or required integration of event features
within the same modality, or across modalities.
Results: Participants' ability to retrieve context features from across multiple modalities was significantly
reduced after AnG stimulation compared to stimulation of the vertex. This effect was observed only for
the integration of cross-modal context features but not for integration of features within the same
modality, and could not be accounted for by task difficulty as performance was matched across integration
conditions following vertex stimulation.
Conclusion: These results support the hypothesis that AnG is necessary for the multimodal integration of
distributed cortical episodic features into a unified conscious representation that enables the experience
of remembering.
... Likewise, our relation trials may be more allocentric insofar as the locations must be maintained in relation to each other (i.e., the relation between the two or three circles). Indeed it has been shown that allocentric shortterm memory is impaired in patients with bilateral hippocampal lesions, but egocentric short-term memory is spared (Holdstock et al., 2000). This is consistent with our results here that show that areas in the MTL are more active for maintaining spatial relations compared to locations. ...
Previous work has demonstrated a distinction between maintenance of two types of spatial information in working memory (WM): spatial locations and spatial relations. While a body of work has investigated the neural mechanisms of sensory-based information like spatial locations, little is known about how spatial relations are maintained in WM. In two experiments, we used fMRI to investigate the involvement of early visual cortex in the maintenance of spatial relations in WM. In both experiments, we found less quadrant-specific BOLD activity in visual cortex when a single spatial relation, compared to a single spatial location, was held in WM. Also across both experiments, we found a consistent set of brain regions that were differentially activated during maintenance of locations vs. relations. Maintaining a location, compared to a relation, was associated with greater activity in typical spatial WM regions like posterior parietal cortex and prefrontal regions. Whereas maintaining a relation, compared to a location, was associated with greater activity in the parahippocampal gyrus and precuneus/retrosplenial cortex. Further, in Experiment 2 we manipulated WM load and included trials where participants had to maintain three spatial locations or relations. Under this high load condition, the regions sensitive to locations vs. relations were somewhat different than under low load. We also identified regions that were sensitive to load specifically for location or relation maintenance, as well as overlapping regions sensitive to load more generally. These results suggest that the neural substrates underlying WM maintenance of spatial locations and relations are distinct from one another and that the neural representations of these distinct types of spatial information change with load.
... First, patients who suffered from developmental topographical disorders (DTD) have damages to the hippocampus (in addition to the retrosplenial cortex, fusiform gyrus, and lingual gyrus) and show impaired performance on navigation tasks (Aguirre and D'Esposito, 1999;Iaria and Barton, 2010). Damages to the hippocampus also result in a deficit in spatial working memory (Abrahams et al., 1997;Bohbot et al., 1998;Holdstock et al., 2000). Second, neuroimaging studies found that the hippocampus is activated by navigation tasks (Maguire et al., 1998;Mellet et al., 2000;Hartley et al., 2003;Iaria et al., 2003Iaria et al., , 2008 and spatial memory tasks (Maguire, 1997;Burgess et al., 2002). ...
Behavioral studies have reported that males perform better than females in 3-dimensional (3D) mental rotation. Given the important role of the hippocampus in spatial processing, the present study investigated whether structural differences in the hippocampus could explain the sex difference in 3D mental rotation. Results showed that after controlling for brain size, males had a larger anterior hippocampus, whereas females had a larger posterior hippocampus. Gray matter volume (GMV) of the right anterior hippocampus was significantly correlated with 3D mental rotation score. After controlling GMV of the right anterior hippocampus, sex difference in 3D mental rotation was no longer significant. These results suggest that the structural difference between males’ and females’ right anterior hippocampus was a neurobiological substrate for the sex difference in 3D mental rotation.
... Individuals using an allocentric strategy in a virtual navigation task show greater activation in the hippocampus, parahippocampal region, and thalamus compared to individuals who use an egocentric strategy (310). Furthermore, hippocampal damage in humans is associated with deficits in allocentric but not egocentric spatial memory (278,279). This is not an exhaustive taxonomy of aspects of spatial cognition but serves to highlight that spatial memory is not a unitary construct. ...
Sex differences in neurological disease exist in incidence, severity, progression, and symptoms and may ultimately influence treatment. Cognitive disturbances are frequent in neuropsychiatric disease with men showing greater cognitive impairment in schizophrenia, but women showing more severe dementia and cognitive decline with Alzheimer's disease. Although there are no overall differences in intelligence between the sexes, men, and women demonstrate slight but consistent differences in a number of cognitive domains. These include a male advantage, on average, in some types of spatial abilities and a female advantage on some measures of verbal fluency and memory. Sex differences in traits or behaviors generally indicate the involvement of sex hormones, such as androgens and estrogens. We review the literature on whether adult levels of testosterone and estradiol influence spatial ability in both males and females from rodent models to humans. We also include information on estrogens and their ability to modulate verbal memory in men and women. Estrone and progestins are common components of hormone therapies, and we also review the existing literature concerning their effects on cognition. We also review the sex differences in the hippocampus and prefrontal cortex as they relate to cognitive performance in both rodents and humans. There has been greater recognition in the scientific literature that it is important to study both sexes and also to analyze study findings with sex as a variable. Only by examining these sex differences can we progress to finding treatments that will improve the cognitive health of both men and women. © 2016 American Physiological Society. Compr Physiol 6:1295-1337, 2016.
... Evidence for the existence of multiple memory systems has also been observed in humans; as in rodents, spatial memory is associated with fMRI activity and grey matter in the hippocampus whereas response memory is associated with the caudate nucleus (Bohbot et al., 2007(Bohbot et al., , 2004Iaria et al., 2003). Increased hippocampal volume is associated with navigational expertise (Maguire et al., 2000;Woollett and Maguire, 2011), and individuals with a damaged hippocampus were shown to have impaired spatial memory (Bohbot et al., 1998;Holdstock et al., 2000). Yet a damaged hippocampus does not impair the use of a response strategy to solve the task (Bohbot et al., 2004). ...
Different memory systems are employed to navigate an environment. It has been consistently shown in rodents that estrogen impacts multiple memory system bias such that low estradiol (E2) is associated with increased use of a striatal-mediated response strategy whereas high E2 increases use of a hippocampal-dependent spatial memory. Low E2 also enhances performance on a response-based task whereas high E2 levels improve learning on a spatial task. The purpose of the present cross-sectional study was to investigate navigational strategies in young, healthy, naturally cycling women. Participants were split into either an early follicular (i.e., when E2 levels are low), ovulatory (i.e., when E2 levels are high) or mid/late luteal (i.e., end of the cycle, when E2 levels decrease and progesterone levels rise) phase group, using self-reported date of the menstrual cycle. Serum hormone level measurements (E2, progesterone, testosterone) were used to confirm cycle phase assignment. Participants were administered a verbal memory task as well as a virtual navigation task that can be solved by using either a response or spatial strategy. Women tested in the ovulatory phase, under high E2 conditions, performed better on a verbal memory task than women tested during the other phases of the cycle. Interestingly, women tested in the mid/late luteal phase, when progesterone is high, predominantly used a spatial strategy, whereas the opposite pattern was observed in the early follicular and ovulatory groups. Our data suggest that the specific memory system engaged differs depending on the phase of the menstrual cycle and may be mediated by both E2 and progesterone, rather than E2 alone.
The hippocampus (HPC) and retrosplenial cortex (RSC) are key components of the brain's memory and navigation systems. Lesions of either region produce profound deficits in spatial cognition and HPC neurons exhibit well‐known spatial firing patterns (place fields). Recent studies have also identified an array of navigation‐related firing patterns in the RSC. However, there has been little work comparing the response properties and information coding mechanisms of these two brain regions. In the present study, we examined the firing patterns of HPC and RSC neurons in two tasks which are commonly used to study spatial cognition in rodents, open field foraging with an environmental context manipulation and continuous T‐maze alternation. We found striking similarities in the kinds of spatial and contextual information encoded by these two brain regions. Neurons in both regions carried information about the rat's current spatial location, trajectories and goal locations, and both regions reliably differentiated the contexts. However, we also found several key differences. For example, information about head direction was a prominent component of RSC representations but was only weakly encoded in the HPC. The two regions also used different coding schemes, even when they encoded the same kind of information. As expected, the HPC employed a sparse coding scheme characterized by compact, high contrast place fields, and information about spatial location was the dominant component of HPC representations. RSC firing patterns were more consistent with a distributed coding scheme. Instead of compact place fields, RSC neurons exhibited broad, but reliable, spatial and directional tuning, and they typically carried information about multiple navigational variables. The observed similarities highlight the closely related functions of the HPC and RSC, whereas the differences in information types and coding schemes suggest that these two regions likely make somewhat different contributions to spatial cognition.
Sex differences in navigation have been a topic of investigation for decades and has been subjected to various contradictory findings and debates. The aim of this work was to compare the spatial memory of men and women tested in various different types of spatial tasks, while controlling for navigation strategies and aging. It is generally thought that men outperform women in navigation and that women have higher scores on object location tasks. However, many studies fail to control for different factors that may bias one sex or the other. We aggregated the data of 465 participants (349 young adults, 127 older adults) who took part in various studies conducted in our laboratory, which include both published and original unpublished data, in order to investigate sex differences. In these studies, we used a number of different paradigms: virtual radial arm mazes, a virtual wayfinding task, an object location task, a virtual Morris Water Maze, and the invisible sensor task which is a real-life model of the Morris Water Maze. While our results may seem discordant at first glance, they demonstrate that several factors can impact the performance of men and women on spatial tasks, including spontaneous navigation strategies, environmental characteristics, and age. We replicated findings showing that women favor proximal landmarks compared to men who favor distal landmarks, women have better memory than men for the position of objects in the absence of reference frames, but they will have poorer scores when navigation requires specific angles, distances and polar coordinates. Moreover, we found that in aging, women who avoid the use of landmarks when navigating a radial maze show stronger reliance on these non-spatial strategies than men. On the other hand, women who rely on landmarks, do so to the same extent as men. Our findings highlight the need to carefully take into consideration these factors in order to produce a more harmonious understanding of sex differences in navigation. Finally, the interaction between spontaneous navigation strategies, sex, and age is discussed in terms of its implications for risk of Alzheimer’s disease.
Aunque los mecanismos moleculares responsablesdel almacenamiento de informacióna largo plazo todavía no se handeterminado en detalle, todo parece indicarque el lóbulo temporal medio juega unpapel crítico en la formación de la memoriadeclarativa. El objetivo de este artículoes realizar una revisión sobre la contribuciónde la investigación en neuropsicologíahumana y de los estudios de lesión yneuroanatómicos en el primate al conocimientode la organización de la memoriadeclarativa.
Spatial navigation and event memory (termed episodic memory) are thought to be heavily intertwined, both in terms of their cognitive processes and underlying neural systems. Some theoretical models posit that both memory for places during navigation and episodic memory depend on highly overlapping brain systems. Here, we assessed this relationship by testing navigation in an individual with severe retrograde and anterograde amnesia; the amnesia stemmed from bilateral lesions in the medial temporal lobes from two separate strokes. The individual with amnesia and age-matched controls were tested on their memories for the locations of previously seen objects relative to distal mountain cues in an immersive virtual environment involving free ambulation. All participants were tested from both repeated and novel start locations and when a single distal mountain cue was unknowingly moved to determine if they relied on a single (beacon) cue to a greater extent than the collection of all distal cues. Compared to age-matched controls, the individual with amnesia showed no significant deficits in navigation from either the repeated or novel start points, although both the individual with amnesia and controls performed well above chance at placing objects near their correct locations. The individual with amnesia also relied on a combination of distal cues in a manner comparable to age-matched controls. Despite largely intact memory for locations using distal cues, the individual with amnesia walked longer paths, rotated more, and took longer to complete trials. Our findings suggest that memory for places during navigation and episodic memory may involve partially dissociable brain circuits and that other brain regions outside of the medial temporal lobe partially support some aspects of navigation. At the same time, the fact that the individual with amnesia walked more circuitous paths and had dense amnesia for autobiographic events supports the idea that the hippocampus may be important for binding information as part of a larger role in memory.
L’étude de la capacité qu’ont les patients amnésiques d’apprendre de nouvelles informations sémantiques connaît un regain d’intérêt depuis une dizaine d’années, notamment suite aux travaux de Vargha-Khadem et collaborateurs (1997) et à l’impact de ceux-ci tant sur notre compréhension des relations entre mémoire sémantique et mémoire épisodique que sur la manière d’envisager, au plan clinique, la prise en charge de ces patients. Cette revue de littérature a pour but de présenter l’état de nos connaissances sur ce sujet, en cherchant à répondre à différentes questions. Quelles sont les relations entre mémoire épisodique et mémoire sémantique ? En quoi l’étude de patients amnésiques peut-elle apporter des éléments de réponses dans ce débat ? Les patients amnésiques peuvent-ils véritablement apprendre de nouvelles informations sémantiques ? Et si oui, quelle est l’étendue et la nature des connaissances qu’ils peuvent acquérir ?
Résumé Avec l’approfondissement de la notion de carte cognitive spatiale, différents paramètres ont été identifiés comme jouant un rôle dans les processus d’encodage de la représentation de l’espace au sein des référentiels de types égo et allocentrés. L’activité du sujet et la nature de la configuration environnementale se révèlent alors être des facteurs déterminants de cet encodage. Bien que les travaux dans ce domaine ne s’accordent pas systématiquement, il semble que les actions du sujet participent à l’intégration de repères centrés sur lui-même alors que les caractéristiques géométriques propres aux configurations tendent à favoriser l’intériorisation de références externes. La coordination de ces encodages de types égo et allocentrés s’impose comme une clé de la réussite des tâches spatiales. Cette note théorique vise à préciser le rôle joué par les mouvements du sujet, sa désorientation, son point de vue initial d’apprentissage, l’axe intrinsèque à la configuration ainsi que la régularité de sa forme dans la coordination des représentations de types égo et allocentrés.
The brain normally adapts to various extents of reactive oxygen species (ROS) and reactive nitrogen species (RNS) within its complex network of neurons and glial cells and, thereby, maintains the neuronal circuits. Although the neuron is the highest consumer of O2 and glucose, it has compromised responses to oxidative stress and nitrative stress, resulting in overwhelming levels of oxidants in the ageing brain. More specifically, the neurons face challenges posed by high levels of free radicals, alterations in mitochondrial metabolism, and calcium signalling, accompanied by overloading of iron at various sites in the brain. The brain has the least antioxidant defences against oxidants, compared to the heart, and previous studies from our group have revealed that the ageing brain is challenged with an accumulation of several oxidised products, resulting in neuronal degeneration and deficits in cognitive functions. Here, we review the findings on redox homeostasis in an ageing brain, which when disturbed by ROS and RNS, paves the way to neurodegenerative diseases that also influence the longevity of the patient. The possibilities of certain non-invasive interventions in offering protection against OS-mediated redox dyshomeostasis in the aged brain are also addressed.
People can navigate in a new environment using multiple strategies dependent on different memory systems. A series of studies have dissociated between hippocampus-dependent “spatial” navigation and habit-based “response” learning mediated by the caudate nucleus. The val66met polymorphism of the brain-derived neurotrophic factor (BDNF) gene leads to decreased secretion of BDNF in the brain, including the hippocampus. Here, we aim to investigate the role of the BDNF val66met polymorphism on virtual navigation behavior and brain activity in healthy older adults. 139 healthy older adult participants (mean age = 65.8 ± 4.4 yrs) were tested in this study. Blood samples were collected and BDNF val66met genotyping was performed. Participants were divided into two genotype groups: val homozygotes and met carriers. Participants were tested on virtual dual-solution navigation tasks in which they could either use a hippocampus-dependent spatial strategy or a caudate nucleus-dependent response strategy to solve the task. A subset of the participants (n = 66) were then scanned in a 3T fMRI scanner while engaging in another dual-solution navigation task. BDNF val/val individuals and met carriers did not differ in learning performance. However, the two BDNF groups differed in learning strategy. BDNF val/val individuals relied more on landmarks to remember target locations (i.e., increased use of flexible spatial learning) while met carriers relied more on sequences and patterns to remember target locations (i.e., increased use of inflexible response learning). Additionally, BDNF val/val individuals had more fMRI activity in the hippocampus compared to BDNF met carriers during performance on the navigation task. This is the first study to show in older adults that BDNF met carriers use alternate learning strategies from val/val individuals and to identify differential brain activation of this behavioral difference between the two groups.
Representations of space in mind are crucial for navigation, facilitating processes such as remembering landmark locations, understanding spatial relationships between objects, and integrating routes. A significant problem, however, is the lack of consensus on how these representations are encoded and stored in memory. Specifically, the nature of egocentric and allocentric frames of reference in human memory is widely debated. Yet, in recent investigations of the spatial domain across the lifespan, these distinctions in mnemonic spatial frames of reference have identified age‐related impairments. In this review, we survey the ways in which different terms related to spatial representations in memory have been operationalized in past aging research and suggest a taxonomy to provide a common language for future investigations and theoretical discussion.
This article is categorized under:
• Psychology > Memory
• Neuroscience > Cognition
• Psychology > Development and Aging
Abstract
Space can be represented from a variety of perspectives, called spatial frames of reference. Whether spatial information is stored in human memory within these frames of reference—called “egocentric” and “allocentric”—is highly debated. In this review, we present a global taxonomy for spatial memory representations to encourage a common language in future research, using cognitive aging as a case study to support this aim.
Spatial memory is an essential ability for living. Some studies have demonstrated the finding of sex differences in spatial memory. However, the results are diverse, ranging from “significant difference” to “no difference”. In this study, we sought to determine the underlying sex differences observed during spatial memory by examining neurofunctional differences in the distinct cortical regions that lay within the spatial memory network. Functional magnetic resonance imaging (fMRI) was used to measure neural responses while healthy young adults were engaged in spatial memory tasks with different levels of memory load. Our results not only illustrate consistent spatial memory networks between the female and male groups but also find a functional interaction between sex and difficulty in left superior frontal gyrus (lSFG) during the encoding phase. In addition, sex divergences in spatial memory appear when task difficulty increases. In sum, our study supports the existence of sex differences in spatial memory and demonstrates the role of task-difficulty expressed in terms of spatial memory involvement.
Neurological amnesia has been and remains the focus of intense study, motivated by the drive to understand typical and atypical memory function and the underlying brain basis that is involved. There is now a consensus that amnesia associated with hippocampal (and, in many cases, broader medial temporal lobe) damage results in deficits in episodic memory, delayed recall, and recollective experience. However, debate continues regarding the patterns of preservation and impairment across a range of abilities, including semantic memory and learning, delayed recognition, working memory, and imagination. This brief review highlights some of the influential and recent advances in these debates and what they may tell us about the amnesic condition and hippocampal function.
La désorientation spatiale est un signe clinique précurseur de la maladie d'Alzheimer. Pour aborder ce sujet, nous nous sommes tout d'abord intéressés à l'orientation spatiale normale. Après un bref rappel des généralités de la maladie d'Alzheimer, nous avons tenté de décrire les multiples mécanismes complexes de la navigation, mis en jeu physiologiquement. Puis nous avons exposé les hypothèses fonctionnelles de la défaillance de l'orientation topographique chez les Alzheimériens, les moyens de les mettre en évidence ainsi que les possibilités d'établir un programme de réhabilitation. L'hippocampe est la structure cérébrale impliquée dans la navigation spatiale à grande échelle et la construction d'une carte mentale de l'espace. Il existe trois types de stratégies cognitives pour se déplacer efficacement. Elles sont organisées de façon hiérarchique, ce sont les points de repère, les routes, et les configurations ou survols. Pour localiser un objet, l'Homme utilise selon ses besoins, soit un cadre égocentrique (centré par rapport à l'individu) soit un cadre exocentrique (par rapport aux objets environnants). Les hypothèses fonctionnelles de la désorientation topographique dans la maladie d'Alzheimer sont nombreuses. La principale est le déclin de la mémoire épisodique, responsable de la mémoire topographique. Nous avons détaillé l'ensemble des fonctions cognitives défaillantes, ainsi que les différents tests pour les évaluer et les techniques de réhabilitation possibles. Enfin, compte tenu des difficultés qu'engendre la désorientation topographique au quotidien, nous avons proposé un protocole d'évaluation de l'orientation spatiale au sein de nouvelles structures sécurisées dans les enceintes hospitalières, les jardins thérapeutiques.
Much of the richness in human life derives from episodic memory, mental representations of detailed experiences from our personal pasts. To make sense of those experiences, knowledge about the world and oneself must also exist in a form that is free of context – known as semantic memory. This chapter revisits and builds on Tulving's distinction between episodic and semantic memory, with a focus on their differences, similarities, and interactions, informed by cognitive, neuropsychological, and neuroimaging studies. Extensions of this distinction into spatial memory, and beyond memory into future thinking, are considered in the context of process views of memory organization.
Our understanding of human amnesia has been greatly advanced through the use of animal models. Although animals and humans differ greatly in many ways, the basic principles of brain organization and function are homologous. The use of selective methods of lesion production has enabled neuroscientists to examine in rats and monkeys the contribution of specific structures implicated in human memory in a way that is rarely possible in human studies. This chapter describes several categories of animal model that have advanced our understanding of the processes underlying normal human memory and, in particular, the deficits observed in human amnesia.
This study assessed age differences in navigational behavior in a virtual Morris water maze (vMWM) and examined the ability of older adults to develop cognitive maps after vMWM experience. Compared with younger participants, older volunteers traversed a longer linear distance to locate the hidden platform. On the probe trial, younger volunteers spent a greater proportion of their total distance traveled in proximity to the platform and had more platform intersections. Analysis of map reproductions demonstrated that older participants used proximal objects to locate the goal but did not use room-geometry cues to aid navigation. These findings demonstrate age-related deficits on a laboratory measure of place learning and suggest that deficiencies in allocentric mapping may contribute to these deficits.
Many neuropsychological investigations of human memory have focused on the amnesic deficits of alcoholic Korsakoff's syndrome. Structural neuroimaging suggests that the syndrome results from midline diencephalic damage, but functional neuroimaging has the potential to reveal additional neuropathology that may be responsible for cognitive dysfunction. Accordingly, high-resolution positron emission tomography (PET) was used to measure regional cerebral metabolic rates for glucose utilization in five alcoholic Korsakoff patients and nine alcoholic control subjects. Results from a continuous recognition test administered during the radiotracer uptake period indicated that all subjects performed normally with respect to immediate memory, whereas Korsakoff patients demonstrated a marked memory impairment in delayed recognition. PET results from the Korsakoff group showed a widespread decline in glucose metabolism in frontal, parietal, and cingulate regions, suggesting that these functional abnormalities in the cerebral cortex contribute to the memory impairment. Hippocampal glucose metabolism did not differ between the groups. Thus, the evidence did not support the hypothesis that parallel brain dysfunctions are responsible for the similar amnesic symptomatology after hippocampal and diencephalic damage. We hypothesize that the amnesic dysfunction of Korsakoff's syndrome depends on a disruption of thalamocortical interactions that mediate a function critical for normal memory storage.
Three experiments investigated how space is represented in the primate hippocampus by recording the activity of single neurons in the hippocampus of behaving macaque monkeys. In Exp 1, Ss had to remember a stimulus and its position. Neurons that responded differently according to the position on a screen in which the stimulus was shown were analyzed for their spatial fields. In the primate hippocampus many spatial cells (69% of those analyzed) responded in relation to allocentric coordinates. Exp 2 showed that very few hippocampal cells were responsive in a fixation spot stimulus task, and that for the cells that did respond, the encoding was not retinotopic. In Exp 3, it was found that relatively many hippocampal neurons (17%) responded differently according to the spatial position being fixated on the screen. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
The neural basis of navigation by humans was investigated with functional neuroimaging of brain activity during navigation
in a familiar, yet complex virtual reality town. Activation of the right hippocampus was strongly associated with knowing
accurately where places were located and navigating accurately between them. Getting to those places quickly was strongly
associated with activation of the right caudate nucleus. These two right-side brain structures function in the context of
associated activity in right inferior parietal and bilateral medial parietal regions that support egocentric movement through
the virtual town, and activity in other left-side regions (hippocampus, frontal cortex) probably involved in nonspatial aspects
of navigation. These findings outline a network of brain areas that support navigation in humans and link the functions of
these regions to physiological observations in other mammals.
A TV/computer technique was used to simultaneously track a rat's position in a simple apparatus and record the firing of single hippocampal complex-spike neurons. The primary finding is that many of these neurons behave as "place cells," as first described by O'Keefe and Dostrovsky (1971) and O'Keefe (1976). Each place cell fires rapidly only when the rat is in a delimited portion of the apparatus (the cell's "firing field"). In agreement with O'Keefe (1976) and many other authors, we have seen that the firing of place cells is highly correlated with the animal's position and is remarkably independent of other aspects of the animal's behavioral state. Several properties of firing fields were characterized. Firing fields are stable over long time intervals (days) if the environment is constant. They come in several shapes when the animal is in a cylindrical apparatus; moreover, the set of field shapes is different when the animal is in a rectangular apparatus. It also seems that a single cell may have more than one field in a given apparatus. By collecting a sample of 40 place cells in a fixed environment, it has been possible to describe certain features of the place cell population, including the spatial distribution of fields within the apparatus, the average size of fields, and the "intensity" of fields (as measured by maximum firing rate). We also tested the hypothesis that the firing rate of each place cell signals the animal's distance from a point (the field center) so that a weighted average of the firing of the individual cells encodes the animal's position within the apparatus. The animal's position, calculated according to this "distance hypothesis," is systematically different from the animal's true position; this implies that the hypothesis in its simplest form is wrong.
Gave 40 rhesus monkeys dorsolateral prefrontal, posterior parietal, or inferotemporal lesions. 4 additional Ss served as unoperated controls. Ss then received 2 forms of spatial discrimination training, based on body position ("egocentric" cues) and on the position of an external referent ("allocentric" cues), respectively. On the former, a place discrimination reversal, frontal Ss were impaired but not parietals. On the latter, a landmark discrimination reversal, parietal Ss were impaired but not frontals; this result was also obtained on a test involving distance discrimination without reversal. Finally, the inferotemporals but not the frontals or parietals were impaired on a nonspatial object discrimination reversal. Results suggest that the 2 modes of spatial orientation, egocentric and allocentric, are related to frontal and parietal mechanisms, respectively. (18 ref.)
Electrophysiological studies have shown that single cells in the
hippocampus respond during spatial learning and
exploration1-4, some firing only when animals enter specific
and restricted areas of a familiar environment. Deficits in spatial
learning and memory are found after lesions of the hippocampus and its
extrinsic fibre connections5,6 following damage to the medial
septal nucleus which successfully disrupts the hippocampal theta
rhythm7, and in senescent rats which also show a correlated
reduction in synaptic enhancement on the perforant path input to the
hippocampus8. We now report, using a novel behavioural
procedure requiring search for a hidden goal, that, in addition to a
spatial discrimination impairment, total hippocampal lesions also cause
a profound and lasting placenavigational impairment that can be
dissociated from correlated motor, motivational and reinforcement
aspects of the procedure.
The present study compared the recognition memory deficit in different groups of amnesics using scores from a standard test. The data, taken from a literature search, came from 33 studies reporting the performance of amnesic subjects on the recognition memory test (RMT) [77]. A total of 112 amnesic subjects were grouped according to their pathology. In addition, the analysis included subjects with schizophrenia, amygdala damage, or frontal lobe damage. Of these three nonamnesic groups, only the frontal lobe subjects were impaired on both RMT subtests, while the schizophrenics showed a disproportionate impairment for the recognition of faces. The amygdala subjects were also poor at face recognition. Among the amnesic groups, those subjects likely to have multiple sites of pathology (e.g. Korsakoff amnesics, post-encephalitics) were found to be the most impaired on the RMT. In contrast, those amnesics with more focal, limbic lesions in the hippocampus, fornix, or mamillary body region showed much milder deficits on the RMT task, some performing at normal levels. Despite their apparent sparing of recognition, the overall severity of amnesia in those subjects with limbic lesions appeared comparable to that in the remaining amnesics. These findings indicate that deficits on both subtests of the RMT are a frequent but not inevitable component of anterograde amnesia. They also point to a distinct subgroup of amnesias associated with selective damage in the hippocampus or its diencephalic targets, in which there is a relative sparing of recognition under certain test conditions.
Recent research indicates that the hippocampus (HC) in animals is involved in memory. A new test for rat memory is described (the dispatch task). The information about the location of the goal is given to S when it is in the startbox. The memory formed is long lasting and Ss remember the location of the goal and not the response to be made to reach that goal. The spatial relations of the cues within the environment can be manipulated to bias Ss toward selection of a place or a guidance hypothesis. The latter does not seem to support long-term memory formation in the way that the former does. Fornix lesions selectively disrupted performance of the place-biased task, a finding predicted by the cognitive map theory but not by other ideas about HC involvement in memory. (22 ref) (PsycINFO Database Record (c) 2012 APA, all rights reserved)
A hippocampal patient is described who shows preserved item
recognition and simple recognition-based recollection but impaired
recall and associative recognition. These data and other evidence
suggest that contrary to Aggleton & Brown's target article,
Papez circuit damage impairs only complex item-item-context
recollection. A patient with perirhinal cortex damage and a delayed
global memory deficit, apparently inconsistent with A&B's
framework, is also described.
The hippocampus has sometimes been proposed to function as a cognitive map, a memory system that stores information about allocentric space. Work with experimental animals and memory-impaired patients has raised difficulties with this view by showing that the hippocampus is not performing an exclusively spatial function. However, the possibility has remained that the hippocampus plays a special role in spatial memory or a disproportionately large role in spatial memory compared to other kinds of memory. This study compared spatial and nonspatial memory in amnesic patients with lesions of the hippocampal formation or diencephalon. Subjects studied an array of 16 toy objects and were subsequently tested for object recall, object recognition, and memory for the location of the objects. Control subjects were tested after long retention intervals in order to equate their object memory performance with that of the patients. The main finding was that, when the performance of amnesic patients on the object memory tests was matched to the object memory performance of control subjects, spatial memory performance of the amnesic patients also matched the spatial memory performance of the control subjects. The results were the same for the two groups of patients. These findings suggest that the hippocampus is not especially involved in spatial memory. Spatial memory is simply one instance of a broader category of memory that requires the hippocampus. While cognitive mapping in its most abstract sense may describe hippocampal function, our results support alternative formulations, suggesting that the hippocampus is necessary for the rapid acquisition of relational, configural, or declarative (as opposed to purely spatial) information.
Point counting represents a convenient and efficient technique for estimating the area of transects through multiple sclerosis (MS) lesions on magnetic resonance (MR) images obtained for sections through the brain. When sectioning has been performed according to the Cavalieri method, unbiased estimates of the total volume of MR-visible MS plaques can be obtained with a precision of 3–5% in 5–10 min.
Groups of Korsakoff (KS) and non-Korsakoff alcoholics (ALC) and a group of normal volunteers, matched for age and verbal IQ, were tested on traditional neuropsychological tests of frontal lobe function and on computerized tests of planning (the Tower of London task) and spatial working memory. KS demonstrated deficits on the planning task which could not be explained by abnormalities of memory, including spatial span, or by visuoperceptive disturbances. KS were also impaired on the spatial working memory task, in part because of the failure to adopt an organized strategy. ALC exhibited fewer impairments which could not be attributed to deficits in either planning or spatial working memory. On Nelson's modified Wisconsin Card Sorting Task, KS and ALC achieved fewer categories than controls but only KS made perseverative errors. The data suggest that in the alcoholic Korsakoff's syndrome there is a specific disturbance of frontal-lobe function in addition to amnesia. The impairments seen in chronic alcoholics without Korsakoff's syndrome, on the other hand, do not reflect specific frontal dysfunction.
The performances of groups of patients with left, right and bilateral frontal lesions were compared on a battery consisting of two tests presumed to be related specifically to left hemisphere function, two tests presumed to be related specifically to right hemisphere function, and two tests presumed to be related specifically to bilateral frontal lobe function. Eighteen predictions, based on both theoretical considerations and the indications of previous literature, were made concerning the differences in performance to be expected among the three groups.
Men with right, left and bilateral cerebral lesions were required to make right/left judgements under two experimental conditions, in one of which a mental re-orientation of the stimulus was presumed to be required. Schematic drawings of a man were exposed in either an upright or inverted position and, on each trial, one of the hands was marked. The subject's task was to say “right” or “left” depending on the hand marked. The right posterior group made fewer errors than the left posterior group under the upright condition but significantly more under the inverted condition. This result is attributed to their failure to perform an appropriate mental rotation of the inverted stimuli.
Place units in the dorsal hippocampus of the freely-moving rat signal the animal's position in an environment (place field). In the present experiments, thirty four place units were recorded in two different environments: one, a small platform where the rat had received neither training nor reward; the other, an elevated T-maze inside a set of black curtains where the rat had been trained on a place discrimination. The places within the curtained enclosure were specified by four cues (a light, a card, a fan, and a buzzer) in addition to the food. Other cues were eliminated by rotating the maze and the four controlled cues relative to the external world from trial-to-trial.
Some units had place fields in both environments while others only had a place field in one. No relationship could be seen between the place fields of units with fields in both environments.
All twelve units tested extensively in the controlled enclosure had place fields related to the controlled cues. Probe experiments in which only some of the controlled cues were available showed that some of these units were being excited by one or two cues while others were influenced in a more complex way. The fields of these latter units were maintained by any two of the 4 cues and were due to inhibitory influences which suppressed the unit firing over the rest of the maze.
Ninety-six patients with localised cerebral lesions were tested on a task of providing reasonable answers to Cognitive Estimate questions. These questions are ones that can be answered using general knowledge available to almost all subjects, but for which no immediately obvious strategy is available. It was found that patients with frontal lesions gave significantly more bizarre answers than patients with more posterior lesions. This effect is interpreted in terms of Luria's (1966) theory of the planning functions of the frontal lobes.
A 54-item cross-modal visuo-tactile test involving geometrical discriminations in Euclidean, affine, projective and topological space (plane and 3-dimensional) was administered to 7 subjects with commissurotomy, 2 with hemispherectomy, 1 with agenesis of corpus callosum, and to 5 normal controls. Using blind manual stereognosis subjects selected one of a choice of three shapes, screened from sight, that best fitted a set of five different geometrical forms presented together on a panel in free vision. An intuitive apprehension of geometrical relations was involved that did not require formal training in geometry. Findings support a consistent minor hemisphere superiority and disclose orderly differences in left hemisphere capabilities correlated with the different types of geometry.
Single units were recorded from the CA1 field of the hippocampus in the freely-moving rat. They were classified as place units, displace units or others. Place units were defined as those for which the rat's position on the maze was a necessary condition for maximal unit firing. Some of these place units (misplace units) fired maximally when the animal sniffed in a place, either because it found something new there or failed to find something which was usually there. Displace units increased their rates during behaviors associated with theta activity in the hippocampal slow waves. In general these were behaviors which changed the rat's position relative to the environment. The influence of various environmental manipulations (e.g., turning off the room lights) on the firing pattern of the place units was tested and the results suggest that they were not responding to a simple sensory stimulus nor to a specific motor behavior. Nor could the unit firing be due purely to motivational or incentive factors. The results are interpreted as strong support for the cognitive map theory of hippocampal function.
To investigate involvement of the hippocampal formation in spatial information processing, activity of neurons in the hippocampal formation of the conscious monkey was recorded during presentation of various visual and auditory stimuli from several directions around the monkey. Of 1,047 neurons recorded, 106 (10.1%) responded to some stimuli from one or more directions. Of these 106 neurons with directionally differentiating responsiveness, 49 responded to visual stimulation, 35 to auditory stimulation, and 22 to both. Among 81 neurons, each tested with more than 10 different stimuli, one type responded independent of the nature of the stimulus (nonselective, n = 39), and responses of the other type depended on the nature of the stimulus (selective, n = 42). To investigate effects of change in spatial relations between test stimuli and background stimuli fixed on the monkey or fixed in the environment, 59 of 106 neurons were tested while the experimental apparatus holding the stimulus was moved relative to the monkey. Of these 59 neurons, 36 changed their responsiveness; 7 maintained the magnitude of their responses but changed the response direction with the movement of the apparatus, 5 changed direction regardless of the movement, and 24 did not change direction, but decreased or extinguished responses from the preferred direction. Thirty-two of 106 neurons were also tested by rotating the monkey. The directionally differentiating responsiveness of 11 neurons followed the monkey (egocentric neurons), that of 9 remained in place in the environment (allocentric neurons), and responses of 12 were reversibly extinguished when the monkey was rotated. The results suggest that these hippocampal neurons may be involved in identification of relations among various kinds of stimuli in different spatial frameworks (egocentric or allocentric) and this identification may be developed from multiple sensory modalities.
Short-term memory was assessed in two groups of amnesic patients. Six patients had confirmed or suspected damage to the hippocampal formation, and six patients had diencephalic damage as a result of alcoholic Korsakoff's syndrome. Verbal short-term memory was evaluated with seven separate administrations of the standard digit span test in order to obtain a precise measure of short-term memory. Nonverbal short-term memory was evaluated with four tests that assessed apprehension, retention, and the ability to manipulate nonverbal material--all within the span of immediate memory. One of these four tests assessed short-term memory for spatial location. Patients with damage to the hippocampal formation had a digit span equivalent to that of control subjects and also performed normally on the four tests of nonverbal short-term memory. The patients with Korsakoff's syndrome had a marginally low digit span and performed poorly on three of the four nonverbal tasks, a finding consistent with the deficits in attention and visuospatial processing previously described for this patient group. These deficits are likely due to the frontal lobe atrophy typically associated with Korsakoff's syndrome, rather than to diencephalic damage. The results support the view that short-term (immediate) memory, including short-term spatial memory, is independent of the hippocampus.
Twenty-four amnesics, including patients with Korsakoff's disease, post-encephalitic amnesia and amnesia caused by rupture of an anterior communicating artery aneurysm (ACoAA), were compared with 24 matched control subjects on a task in which words were presented in any one of four positions on a computer screen and subjects were instructed to remember both the words and their locations. The patients were tested after more learning opportunity, exposure to shorter lists, and after shorter delays than were their controls in order to match the word recognition performance of the two groups. Under these conditions, the amnesics' ability to locate recognized words was significantly worse than that of their controls. Although there was a tendency for the ACoAA patients to show more severe spatial memory deficits than Korsakoff patients, there was no clear evidence that aetiology of amnesia was a critical determinant of whether spatial memory was more impaired than word recognition. It was concluded that amnesics show a disproportionately severe memory deficit for spatial information that is intentionally encoded as well as for that which is incidentally encoded.
Seventeen amnesics, including patients with Korsakoff's disease, post-encephalitic amnesia and amnesia caused by rupture of an anterior communicating artery aneurysm, were compared with 17 matched control subjects on a task in which 16 nameable shapes were placed on different squares of a 49-square grid. One version of the task tapped free recall and recognition of the shapes and a second version tapped three forms of spatial memory. The patients were tested after more learning opportunity and shorter delays than were the controls so as to match their recognition levels. Under these conditions, the amnesics performed worse than the controls on free recall, location-to-target memory, target-to-location memory and possibly on non-associative spatial memory although this was less impaired than target-to-location memory. Each of the main aetiological subgroups showed these disproportionate deficits to an apparently similar degree. The disproportionate free recall deficit was unrelated to the spatial memory deficits and overall severity of amnesia, and was associated with ageing and signs of frontal lobe dysfunction. The disproportionate spatial memory deficits were unrelated to frontal lobe dysfunction, but the target-to-location memory measure was associated with impairments of recognition and recall of target material. The results are broadly consistent with the context-memory deficit hypothesis of amnesia.
The recall of spatial location in patients with left or right temporal-lobe lesions was studied in two experiments, in which recall was tested either immediately after presentation of an array of objects, or after an intervening verbal task, a spatial task or an unfilled interval. Deficits were found only in patients with right temporal-lobe lesions that included extensive removal of the hippocampal region, and only when recall was tested after a delay. The presence of an intervening task in the delay interval did not accentuate the deficit. The results show that, despite a normal ability to encode location, patients with large right hippocampal lesions demonstrate an abnormally rapid forgetting of such information.
An investigation of the extension of O'KEEFE and NADEL's [The Hippocampus as a Cognitive Map. Oxford University Press, Oxford 1978] theory of hippocampal functioning is described in patients who have undergone unilateral temporal lobectomy for the relief of epilepsy. A new spatial task, incorporating a recall-for-designs test but based on studies of spatial memory and cognitive mapping in animals was devised. Results supported the prediction of temporal lobe structure involvement in the mediation of non-egocentric but not egocentric space, and of the role of right temporal lobe structures in conditions designed to encourage "place" but not "cue" learning strategies. The role of verbal mediation in task performance is also discussed.
Single unit activity was recorded from complex spike cells in the hippocampus of the rat while the animal was performing a spatial memory task. The task required the animal to choose the correct arm of a 4 arm plus-shaped maze in order to obtain reward. The location of the goal arm was varied from trial to trial and was identified by 6 controlled spatial cues which were distributed around the enclosure and which were rotated in step with the goal. On some trials these spatial cues were present throughout the trial (spatial reference memory trials) while on other trials they were present during the first part of the trial but were removed before the rat was allowed to choose the goal (spatial working memory trials). On these latter trials the animal had to remember the location of the cues and/or goal during the delay in order to choose correctly. 55 units were recorded during sufficient reference memory trials for the relationship between their firing pattern and different spatial aspects of the environment to be determined. 33 units had fields with significant relations to the controlled cues while 16 had significant relations to the static background cues, those cues in the environment which did not change position from trial to trial. Of 43 units which could be tested for their relation to the shape of the maze arms themselves, 15 showed such a relationship. Therefore the place units can be influenced by different aspects of the spatial environment but those related to the task requirement appear to be more potent. Interaction effects between the different spatial factors also influenced the firing pattern of some units. Of particular interest was the interaction between the controlled cues and the static background cues found in some cells since this might shed some light on how the hippocampus enables the rat to solve the memory task. 30 units with place fields related to the controlled cues were recorded during successful performance on spatial working memory trials as well as during spatial reference memory trials. The place fields of 90% of these units were maintained during the retention phase of the memory trials. During the recording of some units, other types of trial were given as well. On control trials, the cues were removed before the rat was placed on the maze. These trials provided controls for the potential influence of information left behind by the controlled cues and for the influence of the animal's behaviour on the unit activity.(ABSTRACT TRUNCATED AT 400 WORDS)
Short-term memory and long-term memory for visual stimuli not readily verbalisable were studied in amnesic patients. Decay functions for recall of the location of a single dot stimulus over retention intervals of 0-60 sec were measured in a group of 7 amnesic subjects and 6 matched controls. Recall of the location of 5 randomly positioned dots after 10 learning trials was tested using a 2 min retention interval. It was found that the amnesic patients' performance was not significantly worse on the former, S.T.M. task but showed a significant deficit on the latter, L.T.M. task. in addition, three patients with a selective impairment of auditory verbal S.T.M. were tested. The findings are discussed in relation to comparable tasks of verbal S.T.M. and L.T.M.
The accuracy of geographic orientation was studied in patients with unilateral cerebral disease and control patients. The influence of educational background on performance was also assessed. When educational background was controlled, the patients with brain disease performed more poorly than the controls on tasks requiring the localization of states and cities on a map of the United States and on a verbal test requiring them to indicate the directional relations between places. Educational background showed both an overall influence on performance level and an interaction with diagnostic category, the less well educated patients with brain disease showing a larger difference from their controls than did patients with better education. A “vector” score, reflecting a shift in localization toward the left or right part of the map differentiated between patients with right and left hemisphere disease and suggested neglect of the visual field contralateral to the side of lesion in some of these patients. The relationship between directional bias in geographic orientation and unilateral neglect in simpler spatial localization tasks remains an open question.
Tests of immediate verbal memory span (digit span), immediate memory span for visuospatial location (Corsi block span) and short-term forgetting of words and figures (continuous recognition) were administered to eight alcoholic Korsakoff amnesics, eight alcoholic and eight nonalcoholic control subjects. Korsakoff amnesics had normal immediate memory span for both verbal information and visuospatial location. The performance of control subjects on continuous recognition demonstrated dramatically different patterns of forgetting for words and figures. Amnesics forgot more than control subjects did on both continuous recognition tests, but their patterns of forgetting were equivalent to the patterns of control subjects.
Patients with left or right temporal lobectomies, the amnesic patient H.M. with bilateral mesial temporal-lobe damage, and normal control subjects were tested on the incidental recall of objects and their location, both immediately and after a delay. An impairment was seen for both temporal-lobe groups in the delayed recall of objects, but only for the right temporal-lobe group in immediate and delayed recall of location. The deficits after right temporal lobectomy were contingent upon radical excision of the hippocampal region. On both object-recall and location-recall, H.M. was inferior to the most impaired patients with unilateral temporal lobectomies.
Human forgetting can be much more rapid than previous experiments have indicated. Subjects who do not expect a test after
a filled retention interval can rarely recall three consonants correctly after 2 sec of distraction. If there are two kinds
of memory, primary and secondary, the present technique provides a purer method of studying forgetting from primary memory.
Rats with lesions of the medial prefrontal, posterior parietal, or posterior temporal cortex were tested in five spatial navigation tasks, which varied in egocentric or allocentric demands, a visual discrimination task, and two delayed nonmatching-to-sample tasks. Rats with prefrontal lesions were impaired at every spatial navigation task, whereas rats with posterior parietal lesions had selective spatial navigation impairments. Rats with prefrontal lesions were also impaired at a visual delayed nonmatching-to-sample task, as they were unable to learn the task, even with no delay. The results are consistent with the idea that the basic plan of mammalian cortex includes prefrontal, posterior parietal, and posterior temporal regions, each of which have generally similar functions across mammalian taxa. There are, however, species-typical differences that reflect specific ecological pressures on the development of the different regions.
Brain damage can cause several distinct disorders of explicit memory as well as several disorders of implicit memory. Organic amnesia is the best studied explicit memory disorder. It is a syndrome that can be caused by lesions in (a) the medial temporal lobes, (b) the midline diencephalon, or (c) the basal forebrain. It remains unresolved whether one or several functional deficits underlie the syndrome, how these deficits should be characterised, and what is the exact location of the causal lesions. There is good evidence that amnesics encode information normally so their deficit(s) must be of storage or retrieval processes. If storage is disrupted, then one would expect item-specific implicit memory for certain kinds of novel information to be disrupted in amnesics. Current evidence is unable to indicate conclusively whether or not this prediction is met mainly because indirect memory test performance depends on explicit as well as implicit memory. Storage deficits should also result in accelerated forgetting in amnesic patients. Studies are described which reveal accelerated loss of free recall, but not recognition, for stories and semantically organised word lists in amnesics at delays between 15 s and 10 min. This suggests that amnesia involves a storage deficit for complex contextual associations that possibly occurs in conjunction with one or more other functional deficits.
The current methods to monitor fetal growth in utero are based on ultrasound image measurements which, lacking a proper sampling methodology, may be biased to unknown degrees. The Cavalieri method of stereology guarantees the accurate estimation of the volume of an arbitrary object from a few systematic sections. Non-invasive scanning methods, and magnetic resonance imaging (MRI) in particular, are valuable tools to provide the necessary sections, and therefore offer interesting possibilities for unbiased quantification. This paper describes how to estimate fetal volume in utero with a coefficient of error of less than 5% in less than 5 min, from three or four properly sampled MRI scans. MRI was chosen because it does not use ionizing radiations on the one hand, and it offers a good image quality on the other. The impact of potential sources of bias such as fetal motion, chemical shift and partial voluming artefacts is discussed. The methods are illustrated on four subjects monitored between weeks 28 and 40 of gestation.