Spatial memory, recognition memory, and the hippocampus.
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ABSTRACT:
SUBMITTER: Broadbent NJ
PROVIDER: S-EPMC521976 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:The hippocampus plays a critical role in recognition memory in both monkeys and humans. However, neurophysiological studies have rarely reported recognition memory signals among hippocampal neurons. The majority of these previous studies used variants of the delayed match-to-sample task; however, studies of the effects of hippocampal damage in monkey and humans have shown that another task of recognition memory, the visual paired-comparison, or visual preferential looking task (VPLT), is more sensitive to hippocampal damage than the delayed matching tasks. Accordingly, to examine possible recognition memory signals in the hippocampus, we recorded the activity of 131 hippocampal neurons in two monkeys performing the VPLT. Eighty-eight neurons (67%) responded significantly to stimulus presentation relative to the baseline prestimulus period. A substantial proportion of these visually responsive neurons (36%) showed significant firing-rate modulations that reflected whether stimuli were novel or familiar. Additionally, these firing-rate modulations were correlated with recognition memory performance on the VPLT such that larger modulations by stimulus novelty were associated with better performance. Together, these results provide evidence for a neural signal in the hippocampus that may support recognition memory performance.
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Project description:Detecting novelty is critical to consolidate declarative memories, such as spatial contextual recognition memory. It has been shown that stored memories, when retrieved, are susceptible to modification, incorporating new information through an updating process. Catecholamine release in the hippocampal CA1 region consolidates an object location memory (OLM). This work hypothesized that spatial contextual memory updating could be changed by decreasing catecholamine release in the hippocampal CA1 terminals from the locus coeruleus (LC). In a mouse model expressing Cre-recombinase under the control of the tyrosine hydroxylase (TH) promoter, memory updating was impaired by photoinhibition of the CA1 catecholaminergic terminals from the LC (LC-CA1) but not from the ventral tegmental area (VTA-CA1). In vivo microdialysis confirmed that the extracellular concentration of both dopamine (DA) and noradrenaline (NA) decreased after photoinhibition of the LC-CA1 terminals (but not VTA-CA1) during the OLM update session. Furthermore, DA D1/D5 and beta-adrenergic receptor antagonists disrupted behavior, but only the former impaired memory updating. Finally, photoinhibition of LC-CA1 terminals suppressed long-term potentiation (LTP) induction in Schaffer's collaterals as a plausible mechanism for memory updating. These data will help understand the underpinning mechanisms of DA in spatial contextual memory updating.
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Project description:Neuronal oscillations and cross-frequency interactions in the rat hippocampus relate in important ways to memory processes and serve as a model for studying oscillatory activity in cognition more broadly. We report here that hippocampal synchrony (CA3-CA1 coherence) increased markedly in the low gamma range as rats were exploring novel objects, particularly those for which the rat subsequently showed good memory. The gamma synchrony varied across phases of the theta rhythm such that coherence was highest at the falling slope and trough of the theta wave. Further, the shape of the theta wave was more asymmetric and elongated at the falling slope during exploration of objects for which the rat subsequently showed good memory as compared with objects for which the rat subsequently showed poor memory. The results showed a strong association between event-related gamma synchrony in rat hippocampus and memory encoding for novel objects. In addition, a novel potential mechanism of cross-frequency interactions was observed whereby dynamic alterations in the shape of theta wave related to memory in correspondence with the strength of gamma synchrony. These findings add to our understanding of how theta and gamma oscillations interact in the hippocampus in the service of memory.
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Project description:Recognition memory provides the ability to distinguish familiar from novel objects and places, and is important for recording and updating events to guide appropriate behavior. The hippocampus (HPC) and medial prefrontal cortex (mPFC) have both been implicated in recognition memory, but the nature of HPC-mPFC interactions, and its impact on local circuits in mediating this process is not known. Here we show that novelty discrimination is accompanied with higher theta activity (4-10 Hz) and increased c-Fos expression in both these regions. Moreover, theta oscillations were highly coupled between the HPC and mPFC during recognition memory retrieval for novelty discrimination, with the HPC leading the mPFC, but not during initial learning. Principal neurons and interneurons in the mPFC responded more strongly during recognition memory retrieval compared with learning. Optogenetic silencing of HPC input to the mPFC disrupted coupled theta activity between these two structures, as well as the animals' (male Sprague Dawley rats) ability to differentiate novel from familiar objects. These results reveal a key role of monosynaptic connections between the HPC and mPFC in novelty discrimination via theta coupling and identify neural populations that underlie this recognition memory-guided behavior.SIGNIFICANCE STATEMENT Many memory processes are highly dependent on the interregional communication between the HPC and mPFC via neural oscillations. However, how these two brain regions coordinate their oscillatory activity to engage local neural populations to mediate recognition memory for novelty discrimination is poorly understood. This study revealed that the HPC and mPFC theta oscillations and their temporal coupling is correlated with recognition memory-guided behavior. During novel object recognition, the HPC drives mPFC interneurons to effectively reduce the activity of principal neurons. This study provides the first evidence for the requirement of the HPC-mPFC pathway to mediate recognition memory for novelty discrimination and describes a mechanism for how this memory is regulated.
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Project description:Study objectivesSeveral studies have now demonstrated that spatial information is processed during sleep, and that posttraining sleep is beneficial for human navigation. However, it remains unclear whether the effects of sleep are primarily due to consolidation of cognitive maps, or alternatively, whether sleep might also affect nonhippocampal aspects of navigation (e.g., speed of motion) involved in moving through a virtual environment.DesignParticipants were trained on a virtual maze navigation task (VMT) and then given a memory test following either a day of wakefulness or a night of sleep. Subjects reported to the laboratory for training at either 10:00am or 10:00pm, depending on randomly assigned condition, and were tested 11 h later. Overnight subjects slept in the laboratory with polysomnography.SettingA hospital-based academic sleep laboratory.Patients or participantsThirty healthy college student volunteers.InterventionsN/A.Measurements and resultsPoint-by-point position data were collected from the VMT. Analysis of the movement data revealed a sleep-dependent improvement in maze completion time (P < 0.001) due to improved spatial understanding of the maze layout, which led to a shortening of path from start to finish (P = 0.01) rather than faster exploration speed through the maze (P = 0.7).ConclusionsWe found that overnight sleep benefitted performance, not because subjects moved faster through the maze, but because they were more accurate in navigating to the goal. These findings suggest that sleep enhances participants' knowledge of the spatial layout of the maze, contributing to the consolidation of hippocampus-dependent spatial information.CitationNguyen ND; Tucker MA; Stickgold R; Wamsley EJ. Overnight sleep enhances hippocampus-dependent aspects of spatial memory. SLEEP 2013;36(7):1051-1057.
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Project description:We designed a novel experiment to investigate the modulation of human recognition memory by environmental context. Human participants were asked to navigate through a four-arm Virtual Reality (VR) maze in order to find and memorize discrete items presented at specific locations in the environment. They were later on tested on their ability to recognize items as previously presented or new. By manipulating the spatial position of half of the studied items during the testing phase of our experiment, we could assess differences in performance related to the congruency of environmental information at encoding and retrieval. Our results revealed that spatial context had a significant effect on the quality of memory. In particular, we found that recognition performance was significantly better in trials in which contextual information was congruent as opposed to those in which it was different. Our results are in line with previous studies that have reported spatial-context effects in recognition memory, further characterizing their magnitude under ecologically valid experimental conditions.
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Project description:Vincristine is a commonly used cytostatic drug for the treatment of leukemia, neuroblastoma and lung cancer, which is known to have neurotoxic properties. The aim of this study was to assess the effects of vincristine, injected directly into the dorsal hippocampus, in spatial memory using the spatial cone field discrimination task. Long Evans rats were trained in the cone field, and after reaching training criterion received bilateral vincristine infusions into the dorsal hippocampus. Vincristine-treated animals presented unilateral or bilateral hippocampal lesions. Animals with bilateral lesions showed lower spatial working and reference memory performance than control animals, but task motivation was unaffected by the lesions. Working and reference memory of animals with unilateral lesions did not differ from animals with bilateral lesions and control animals. In sum, intrahippocampal injection of vincristine caused profound tissue damage in the dorsal hippocampus, associated with substantial cognitive deficits.
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Project description:Severe loss of cholinergic neurons in the basal forebrain nuclei and of noradrenergic neurons in the locus coeruleus are almost invariant histopathological hallmarks of Alzheimer's disease. However, the role of these transmitter systems in the spectrum of cognitive dysfunctions typical of the disease is still unclear, nor is it yet fully known whether do these systems interact and how. Selective ablation of either neuronal population, or both of them combined, were produced in developing animals to investigate their respective and/or concurrent contribution to spatial learning and memory, known to be severely affected in Alzheimer's disease. Single or double lesions were created in 4-8 days old rats by bilateral intraventricular infusion of two selective immunotoxins. At about 16 weeks of age, the animals underwent behavioural tests specifically designed to evaluate reference and working memory abilities, and their brains were later processed for quantitative morphological analyses. Animals with lesion to either system alone showed no significant reference memory deficits which, by contrast, were evident in the double-lesioned subjects. These animals could not adopt an efficient search strategy on a given testing day and were unable to transfer all relevant information to the next day, suggesting deficits in acquisition, storage and/or recall. Only animals with single noradrenergic or double lesions exhibited impaired working memory. Interestingly, ablation of cholinergic afferents to the hippocampus stimulated a robust ingrowth of thick fibres from the superior cervical ganglion which, however, did not appear to have contributed to the observed cognitive performance. Ascending cholinergic and noradrenergic afferents to the hippocampus and neocortex appear to be primarily involved in the regulation of different cognitive domains, but they may functionally interact, mainly at hippocampal level, for sustaining normal learning and memory. Moreover, these transmitter systems are likely to compensate for each other, but apparently not via ingrowing sympathetic fibres.
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Project description:The medial temporal lobe (MTL) is widely implicated in supporting episodic memory and navigation, but its precise functional role in organizing memory across time and space remains elusive. Here we examine the specific cognitive processes implemented by MTL structures (hippocampus and entorhinal cortex) to organize memory by using electrical brain stimulation, leveraging its ability to establish causal links between brain regions and features of behavior. We studied neurosurgical patients of both sexes who performed spatial-navigation and verbal-episodic memory tasks while brain stimulation was applied in various regions during learning. During the verbal memory task, stimulation in the MTL disrupted the temporal organization of encoded memories such that items learned with stimulation tended to be recalled in a more randomized order. During the spatial task, MTL stimulation impaired subjects' abilities to remember items located far away from boundaries. These stimulation effects were specific to the MTL. Our findings thus provide the first causal demonstration in humans of the specific memory processes that are performed by the MTL to encode when and where events occurred.SIGNIFICANCE STATEMENT Numerous studies have implicated the medial temporal lobe (MTL) in encoding spatial and temporal memories, but they have not been able to causally demonstrate the nature of the cognitive processes by which this occurs in real-time. Electrical brain stimulation is able to demonstrate causal links between a brain region and a given function with high temporal precision. By examining behavior in a memory task as subjects received MTL stimulation, we provide the first causal evidence demonstrating the role of the MTL in organizing the spatial and temporal aspects of episodic memory.
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Project description:Adult rats with extensive, bilateral neurotoxic lesions of the hippocampus showed normal forgetting curves for object recognition memory, yet were impaired on closely related tests of object recency memory. The present findings point to specific mechanisms for temporal order information (recency) that are dependent on the hippocampus and do not involve object recognition memory. The object recognition tests measured rats exploring simultaneously presented objects, one novel and the other familiar. Task difficulty was varied by altering the retention delays after presentation of the familiar object, so creating a forgetting curve. Hippocampal lesions had no apparent effect, despite using an apparatus (bow-tie maze) where it was possible to give lists of objects that might be expected to increase stimulus interference. In contrast, the same hippocampal lesions impaired the normal preference for an older (less recent) familiar object over a more recent, familiar object. A correlation was found between the loss of septal hippocampal tissue and this impairment in recency memory. The dissociation in the present study between recognition memory (spared) and recency memory (impaired) was unusually compelling, because it was possible to test the same objects for both forms of memory within the same session and within the same apparatus. The object recency deficit is of additional interest as it provides an example of a nonspatial memory deficit following hippocampal damage.
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