Allocentric Spatial Memory Activation of the Hippocampal Formation Measured With fMRI.

Parslow, David; Rose, David; Brooks, Barbara; Fleminger, Simon; Gray, Jeffrey A.; Giampietro, Vincent; Brammer, Michael; Williams, Steven; Gasston, David; Andrew, Christopher; Vythelingum, Goparlen N.; loannou, Glafkos; Simmons, Andrew; Morris, Robin G.

doi:10.1037/0894-4105.18.3.450

Cited by 105 publications

(88 citation statements)

References 64 publications

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“…Recent experiments demonstrate that selective hippocampal damage prevents spatial relational learning in freely moving adult rhesus monkeys (Macaca mulatta) 7 . Studies of human hippocampal function also highlight its involvement with allocentric representations of space [8][9][10][11][12] .Here, we tested the ability of juvenile monkeys that received hippocampal lesions shortly after birth to learn new spatial relational information. Freely moving monkeys were allowed to forage for a preferred food that was hidden beneath cups distributed in an openfield arena (Fig.…”

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Spatial relational learning persists following neonatal hippocampal lesions in macaque monkeys

Lavenex

Amaral³

2006

Nat Neurosci

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The hippocampus is important for the acquisition of spatial representations of the environment and consequently in contextual memory. This suggests that the neural substrates underlying spatial cognition might be essential for remembering specific life episodes. Indeed, hippocampal lesions prevent spatial relational learning in adult rodents and monkeys, and result in profound amnesia in adult humans. In contrast, we show here that monkeys with neonatal hippocampal lesions learned new spatial relational information. Our experiments suggest that early hippocampal damage leads to functional brain reorganization that enables spatial information to be acquired through the use of brain regions that normally do not subserve this function.The hippocampal formation, a group of cortical brain regions located in the medial temporal lobe, is essential for memory function. Behavioral and electrophysiological experiments in rodents have shown that hippocampal integrity is critical for learning and remembering a particular location in the absence of local cues: that is, for forming an allocentric (viewpoint-independent) representation of space that codes the goal location in relation to distant environmental cues [1][2][3][4][5][6] . Recent experiments demonstrate that selective hippocampal damage prevents spatial relational learning in freely moving adult rhesus monkeys (Macaca mulatta) 7 . Studies of human hippocampal function also highlight its involvement with allocentric representations of space [8][9][10][11][12] .Here, we tested the ability of juvenile monkeys that received hippocampal lesions shortly after birth to learn new spatial relational information. Freely moving monkeys were allowed to forage for a preferred food that was hidden beneath cups distributed in an openfield arena (Fig. 1). Six potentially baited cups were located in two arrays of 3 distinct locations among 18 possible locations. Each day, three locations on one of the arrays were baited. Food locations changed pseudo-randomly among arrays between days. The six potentially baited locations were fixed in relation to distant environmental cues. Monkeys were tested in two conditions. In the first, the local cue condition, colored cups identified the potentially baited locations, so that monkeys could rely on either a visual guidance strategy (egocentric coding) 1-6 or spatial relational information (allocentric coding) [1][2][3][4][5][6] to discriminate between the potentially baited and never-baited locations. In the second, the spatial relational condition, all cups were the same neutral color, so that the monkeys had to rely on an allocentric representation of the environment to discriminate between the potentially baited and never-baited locations. Multiple goals and four pseudo-randomly chosen entrance points prevented the monkeys from relying on an egocentric strategy to identify food locations 7,13 .In contrast to monkeys with adult hippocampal lesions 7 , we show that monkeys with neonatal hippocampal lesions showed normal spatial relational le...

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Spatial relational learning persists following neonatal hippocampal lesions in macaque monkeys

Lavenex

Amaral³

2006

Nat Neurosci

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“…self-ordered sequencing | muscimol | temporal lobe | cognition | nonhuman primate A lthough a role for the hippocampus in navigational spatial memory has been well documented in many species, including humans (1)(2)(3)(4), rodents (5,6), and monkeys (7)(8)(9), a role for hippocampus in nonnavigational spatial memory is less certain. Because nonhuman primates have a close neuroanatomical and behavioral homology to humans, they offer a unique opportunity to assess the neural substrates of spatial memory using nonnavigational tasks.…”

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Memory loss in a nonnavigational spatial task after hippocampal inactivation in monkeys

Forcelli

Palchik

Leath³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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The hippocampus has a well-documented role for spatial navigation across species, but its role for spatial memory in nonnavigational tasks is uncertain. In particular, when monkeys are tested in tasks that do not require navigation, spatial memory seems unaffected by lesions of the hippocampus. However, the interpretation of these results is compromised by long-term compensatory adaptation occurring in the days and weeks after lesions. To test the hypothesis that hippocampus is necessary for nonnavigational spatial memory, we selected a technique that avoids long-term compensatory adaptation. We transiently disrupted hippocampal function acutely at the time of testing by microinfusion of the glutamate receptor antagonist kynurenate. Animals were tested on a self-ordered spatial memory task, the Hamilton Search Task. In the task, animals are presented with an array of eight boxes, each containing a food reinforcer; one box may be opened per trial, with trials separated by a delay. Only the spatial location of the boxes serves as a cue to solve the task. The optimal strategy is to open each box once without returning to previously visited locations. Transient inactivation of hippocampus reduced performance to chance levels in a delay-dependent manner. In contrast, no deficits were seen when boxes were marked with nonspatial cues (color). These results clearly document a role for hippocampus in nonnavigational spatial memory in macaques and demonstrate the efficacy of pharmacological inactivation of this structure in this species. Our data bring the role of the hippocampus in monkeys into alignment with the broader framework of hippocampal function.A lthough a role for the hippocampus in navigational spatial memory has been well documented in many species, including humans (1-4), rodents (5, 6), and monkeys (7-9), a role for hippocampus in nonnavigational spatial memory is less certain. Because nonhuman primates have a close neuroanatomical and behavioral homology to humans, they offer a unique opportunity to assess the neural substrates of spatial memory using nonnavigational tasks. However, studies using nonnavigational spatial tasks with nonhuman primates have found little or no effect of hippocampal lesions (10-15).The ability of hippocampal-lesioned monkeys to perform these tasks without impairment has been explained by the reliance on a strategy that is not dependent on hippocampus. Whereas the use of allocentric (world-centered) cues depends on the hippocampus, it is thought that the use of egocentric (body-centered) cues does not. Indeed, it has been suggested that the use of egocentric cues is supported by extrahippocampal substrates including striatum and parietal cortex (15)(16)(17)(18).Following a hippocampal lesion, subjects may learn to resolve a given task by developing a strategy distinct from that used in the presence of an intact hippocampus. Several factors may support this compensatory strategy, including (i) postlesion training or retraining and (ii) postlesion network reorganization (19-21). T...

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“…By combining virtual reality and fMRI it has been shown that the Arena task reliably activates the hippocampus in a predictable way 20 . In this task both age and the muscarinic receptor antagonist, scopolamine, reduce hippocampal activation and impair spatial learning.…”

Section: P1vital Consortium Studies In Cognitive Disordersmentioning

confidence: 99%

Validation of experimental medicine methods in psychiatry: The P1vital approach and experience

Dawson

Craig

Dourish

2011

Biochemical Pharmacology

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Allocentric Spatial Memory Activation of the Hippocampal Formation Measured With fMRI.

Cited by 105 publications

References 64 publications

Spatial relational learning persists following neonatal hippocampal lesions in macaque monkeys

Spatial relational learning persists following neonatal hippocampal lesions in macaque monkeys

Memory loss in a nonnavigational spatial task after hippocampal inactivation in monkeys

Validation of experimental medicine methods in psychiatry: The P1vital approach and experience

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