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PubMed2005

A cellular correlate of learning-induced metaplasticity in the hippocampus.

Metaplasticity, the plasticity of synaptic plasticity, is thought to have a pivotal role in activity-dependent modulation of synaptic connectivity, which underlies learning and memory. Metaplasticity is usually attributed to modifications in glutamate receptor-mediated synaptic transmission. However, experimental evidence and theoretical considerations suggest that learning reduces the predisposition for further synaptic strengthening, while behavioral studies show that learning capability is enhanced by prior learning. Here we show that enhanced neuronal excitability in CA1 pyramidal neurons, but not enhanced synaptic transmission, occurs prior to rule learning of an olfactory discrimination task. This transient enhancement lasts for 1 day after rule learning, is apparent throughout the cell population and results from reduction in the medium and slow after-hyperpolarizations that control spike frequency adaptation. Such olfactory learning-induced increased excitability in hippocampal neurons enhances the rats' learning capability in another hippocampus-dependent task, the Morris water maze. Once olfactory discrimination rule learning is acquired, its maintenance is not dependent on the reduced post-burst AHP in hippocampal neurons. However, the enhanced spatial learning capability of olfactory-trained rats in the water maze is diminished once the post burst AHP in CA1 pyramidal cells resumes its initial value. We suggest that enhanced excitability of CA1 neurons may serve as a mechanism for generalized enhancement of hippocampus-dependent learning capability. In the presence of such enhanced neuronal excitability, the hippocampal network enters into a 'learning mode' in which a variety of hippocampus-dependent skills are acquired rapidly and efficiently.

Animals↗
PubMed1993

Memory impairments following lesions to the mammillary region of the rat.

The contribution of the mammillary region to learning and memory was investigated. It was demonstrated that lesions of this region impair performance on tasks that require memory for spatial information but that the deficit depends both on the amount of damage within the region and the difficulty of the task. A dissociation in the effect of such lesions on performance of comparable spatial and non-spatial memory tasks was shown. In contrast to the deficits observed on spatial memory tasks, the acquisition and retention of a complex non-spatial memory task was not impaired after extensive damage to the mammillary region. Such lesions also did not impair performance in a conditioned taste aversion task. These experiments suggest that the mammillary region may be selectively involved in spatial learning and memory.

Animals↗
PubMed1993

Chronic nicotine ingestion improves radial arm maze performance in rats.

Effects of chronic nicotine treatment on spatial memory were studied in rats. After 3 weeks of administration of 2.5mg/kg/day in drinking water, the rats were submitted to a spatial learning task in an eight-arm radial maze, during which time the treatment was maintained. Chronic nicotine treatment improved daily spatial memory performance after the animals reached an asymptotic level. Nicotine-treated animals showed significantly better performance than control animals regarding the first error and the total correct path choices.

Journal Article↗
PubMed2004

Rodent spatial navigation: at the crossroads of cognition and movement.

Tasks that measure spatial learning and navigation have become central to contemporary research programs concerned with identifying the neurobiological bases of learning and memory. Although the past three decades have seen an explosion of research reports on rodent navigation, only a small proportion of this research has been directly aimed at identifying the constituent psychological and behavioral processes involved in navigation. Such efforts are critical for establishing a complete neuroscientific explanation of spatial behavior and navigation, however, the majority of these research efforts have focused on identifying a single behavioral dissociation (e.g. place learning vs cued navigation). Experimental comparisons limited to only two possible alternatives can lead to erroneous or otherwise incomplete conclusions regarding how animals navigate. Because multiple sources of information may come to bear on an animal's behavior in spatial tasks, consideration of these sources and their interaction may avoid certain pitfalls inherent in the single dissociation approach. We offer a descriptive model of rodent navigation which includes three important dimensions: reference frame, information, and movement control. A variety of extant behavioral and neurophysiological data that support the basic utility of this conceptual framework are discussed.

Animals↗
PubMed2002

Effect of topiramate following recurrent and prolonged seizures during early development.

Topiramate, an antiepileptic drug with a number of mechanisms of action including inhibition of glutamate activity at the AMPA and KA receptors, was assessed as a neuroprotective agent following seizures. We administered topiramate, 80 mg/kg, or saline for 4 weeks following a series of 25 neonatal seizures or status epilepticus (SE) induced by lithium-pilocarpine in postnatal day 20 rats. Age-matched control rats without a history of seizures were administered topiramate or saline. Following completion of the topiramate injections, animals were tested in the water maze for spatial learning and the brains examined for cell loss and sprouting of mossy fibers. While there was a trend for improved visual-spatial performance in the water maze following topiramate therapy in rats with neonatal seizures, no differences were found in the histological examination of the hippocampus. Neonatal rats exposed to 4 weeks of topiramate did not differ from non-treated controls in water maze performance or histological examination. In weanling rats subjected to SE, topiramate provided a moderate degree of neuroprotection, with topiramate-treated rats performing better in the water maze than rats receiving saline. However, no differences in cell loss or mossy fiber sprouting were found in the histological examination of the brains. These findings demonstrate that chronic treatment with topiramate following SE improves cognitive function. In addition, long-term administration of high-dose topiramate in the normal developing rat brain does not appear to impair cognitive performance.

Animals↗
PubMed1998

The cerebellum in the spatial problem solving: a co-star or a guest star?

The experimental findings reviewed here indicate that the cerebellum has to be added to the regions known to be involved in the spatial learning. Cerebellar function is specifically linked to 'how to find an object' rather than 'where the object is in the space'. In the Morris water maze (MWM) hemicerebellectomized (HCbed) rats displayed a severe impairment in coping with spatial information, displaying only peripheral circling. And yet, when the MWM cue phase was prolonged, HCbed rats succeeded in acquiring some abilities to learn platform position, even in a pure place paradigm, such as finding a hidden platform with the starting points sequentially changed. Conversely, whether the searching strategy was acquired preoperatively, no exploration deficit appeared. Thus, cerebellar lesions appear to affect the procedural components of spatial function, sparing the declarative ones. When intact animals were non-spatially pre-trained and then HCbed, they exhibited an expanded scanning strategy, underlining the cerebellar involvement in procedural component acquisition. By testing HCbed rats in an active avoidance task, first without and then with a request for right/left discrimination, lesioned rats displayed severe deficits. Thus, besides a marked impairment in facing procedural components of spatial processing, cerebellar lesion provokes deficits also in right/left discrimination task. In conclusion, it is possible to propose the cerebellum as one part of a large system that includes frontal, posterior parietal, inferior temporal cortices, hippocampus and basal ganglia. These structures form an allocentric spatial system and an egocentric control system, that interlock to process the information involved in representing an object in the space.

Animals↗
PubMed2004

Correlations between hypothalamus-pituitary-adrenal axis parameters depend on age and learning capacity.

Glucocorticoid hormones are released after activation of the hypothalamus-pituitary-adrenal (HPA) axis and in the brain can modulate synaptic plasticity and memory formation. Clear individual differences in spatial learning and memory in the water maze allowed classification of groups of young (3 months) and aged (24 months) male Wistar rats as superior and inferior learners. We tested 1) whether measures of HPA activity are associated with cognitive functions and aging and 2) whether correlations of these measures depend on age and learning performance. Basal ACTH, but not corticosterone, was increased in aged rats, with the stress-induced ACTH response exaggerated in aged-inferior learners. Aged-superior learners had lower expression of glucocorticoid receptor and CRH mRNA in the parvocellular paraventricular nucleus of the hypothalamus compared with all other groups. Hippocampal mineralocorticoid receptor and glucocorticoid receptor mRNAs differed modestly between groups, but steroid receptor coactivator and heat-shock-protein 90 mRNAs were not different. Strikingly, correlations between HPA axis markers were dependent on grouping animals according to learning performance or age. CRH mRNA correlated with ACTH only in aged animals. Parvocellular arginine vasopressin mRNA was negatively correlated to basal corticosterone, except in aged-inferior learners. Corticosteroid receptor mRNA expression showed a number of correlations with other HPA axis regulators specifically in superior learners. In summary, the relationships between HPA axis markers differ for subgroups of animals. These distinct interdependencies may reflect adjusted set-points of the HPA axis, resulting in adaptation (or maladaptation) to the environment and, possibly, an age-independent determination of learning ability.

Adrenal Glands↗
PubMed2000

Chronic [D-Ala2]-growth hormone-releasing hormone administration attenuates age-related deficits in spatial memory.

The age-related decline in growth hormone is one of the most robust endocrine markers of biological aging and has been hypothesized to contribute to the physiological deficits observed in aged animals. However, there have been few studies of the impact of this hormonal decline on brain aging. In this study, the effect of long-term subcutaneous administration of [D-Ala2]-growth hormone-releasing hormone (GHRH) on one measure of brain function, memory, was investigated. Animals were injected daily with 2.3 microg of [D-Ala2]-GHRH or saline from 9 to 30 months of age, and the spatial learning and reference memory of animals were assessed by using the Morris water maze and compared with those of 6-month-old animals. Results indicated that spatial memory decreased with age and that chronic [D-Ala2]-GHRH prevented this age-related decrement (24% improvement in the annulus-40 time and 23% improvement in the number of platform crossings compared with saline treated, age-matched controls; p < .05 each). No changes were noted in sensorimotor performance. [D-Ala2]-GHRH attenuated the age-related decline in plasma concentrations of insulinlike growth factor-1 (IGF-1) (p <.05). These data suggest that growth hormone and IGF-1 have important effects on brain function, that the decline in growth hormone and IGF-1 with age contributes to impairments in reference memory, and that these changes can be reversed by the chronic administration of GHRH.

Aging↗
PubMedDate not supplied

Regional changes in expression of NCAM, GFAP, and S100 in aging rat brain.

In aging brain degenerative processes occur. However, the aging brain still have regenerative capacity although diminished compared to young rats. The neural cell adhesion molecule (NCAM) may be involved in neuroplasticity during regenerative events. In this study, the polypeptide composition and amount of NCAM was determined in regions of brain from young, mature and old rats. During adult life, the amount of NCAM decreased in several brain regions whereas in aged rats, NCAM was enhanced in all brain regions examined. The amount of the glial fibrillary acidic protein (GFAP) increased during aging in all brain regions reflecting general gliosis in the aged rat brain. The amount of the neuro- and gliotrophic protein S100 increased from young adult to mature age in all brain regions investigated followed by a decrease during old age. Aged rats were tested in a Morris water maze and a group of rats (20%) with learning impairment was defined. However, no differences in amount of NCAM, GFAP, or S100 were observed between aged rats with and without spatial learning impairment.

Aging↗
PubMed2005

Morris water maze search strategy analysis in PDAPP mice before and after experimental traumatic brain injury.

Traumatic brain injury (TBI) is a common cause of cognitive dysfunction and a major risk factor for Alzheimer's disease (AD). PDAPP mice, a transgenic line overexpressing a mutant human amyloid precursor protein (APP) implicated in familial AD, have markedly impaired behavioral performance in the Morris water maze relative to wild-type (WT) littermates. Performance further deteriorates following experimental TBI in both PDAPP and WT mice. However, the aspects of cognitive function involved are not well understood. Here, we have analyzed search strategies used in the water maze by 3-4 month old PDAPP and WT C57Bl6 littermates both before and after moderate controlled cortical impact TBI. Prior to TBI, PDAPP mice used less spatial strategies and more nonspatial systematic strategies and strategies involving repetitive looping than WT mice. With training, PDAPP mice used more spatial strategies and less repetitive looping. After TBI, PDAPP mice lost use of spatial strategies and relied more on repetitive looping. TBI in WT mice also reduced their use of spatial strategies but instead caused a switch to nonspatial systematic strategies. We also analyzed changes in the efficiency with which mice used each individual strategy, but found that differences in which strategies were used quantitatively accounted for most of the differences in performance between groups. These results demonstrate that suboptimal search strategy use in addition to effects on spatial learning and memory underlies the impaired performance of PDAPP mice and further deterioration following TBI. Human TBI patients may have analogous poor use of problem solving strategies.

Amyloid beta-Protein Precursor↗
PubMed2003

GABA(A) receptor subtype selective cognition enhancers.

Currently the treatment of Alzheimer's disease (AD) and Mild Cognitive Impairment (MCI) is largely unrealised, with no preventive or curative therapies. The marketed acetylcholinesterase inhibitors (eg. donepezil, Aricept) are directed toward temporary symptomatic relief from impaired cognition, but have prominent adverse effects with minimal efficacy. In pursuit of novel cognition enhancers, the observation that classical benzodiazepines (BZ, eg. diazepam) are amnesic, coupled with the preservation of GABA(A) receptors in brain areas most affected by AD, highlighted the GABA(A) receptor as a potential therapeutic target. In contrast to the amnesic BZ agonists, the BZ inverse agonists (eg. DMCM) which attenuate GABA(A) receptor function, have been shown to improve performance in animal models of learning and memory. Unfortunately, such non-selective ligands also induce anxiety and convulsions. More recently, novel ligands have been developed (eg. 6,6-dimethyl-3-(2-hydroxyethyl)thio-1-(thiazol-2-yl)-6,7-dihydro-2-benzothiophen-4(5H)-one) that demonstrate binding selectivity and high inverse agonism for the alpha5 GABA(A) receptor subtype, which is preferentially located in the hippocampus, a region of the brain associated with learning and memory. Pre-clinical results are encouraging, since these alpha5 selective inverse agonists enhance memory in animal models, such as spatial learning in the Morris water-maze, but are devoid of the adverse effects associated with activity at other GABA(A) receptor subtypes in other brain regions. If the efficacy and safety profiles of alpha5 inverse agonists in humans prove to be similar to those seen in pre-clinical studies, these compounds would offer significant benefit to AD and MCI patients.

Alzheimer Disease↗
PubMed2001

Grafting neural stem cells improved the impaired spatial recognition in ischemic rats.

To determine the possible therapeutic potential of neural stem cells (NSCs) introduced into the damaged central nervous system, we grafted adult hippocampus-derived NSCs into the hippocampus of rats with transient global ischemia. Transient four-vessel occlusion yielded 90-95% losses of pyramidal neurons in the hippocampal CA1 region. In this region, 1-3% of the grafted cells survived; and 3-9% of them expressed NeuN, a neuronal marker. Rats with more than 120 NeuN-positive cells showed partial improvement of impaired spatial learning in a water maze test. These results suggest that NSCs grafted in the ischemic brain are able to differentiate into neurons and to improve spatial recognition.

Animals↗
PubMed2002

Place-cell impairment in glutamate receptor 2 mutant mice.

There is a strong correlation between Hebbian, NMDA receptor-dependent long-term potentiation (LTP), place-cell firing, and learning and memory. We made glutamate receptor 2 (GluR2) null mutant mice that show enhanced non-Hebbian LTP in hippocampal CA1 neurons and impaired performance in a spatial learning task. We concluded that in vivo hippocampal place cells of GluR2 mutant mice were functionally impaired because (1) only 22.6% of CA1 neurons showed place fields in GluR2 mutant mice, which was significantly lower than that (43.8%) in wild-type mice; (2) GluR2 mutant place fields were much less precise; and (3) GluR2 mutant place fields were extremely unstable. Our data suggest that place cells of GluR2 knock-out mice did not form robust place fields, and that enhanced non-Hebbian LTP might play a negative role in their formation.

Action Potentials↗
PubMed2005

Vestibular influence on water maze retention: transient whole body rotations improve the accuracy of the cue-based retention strategy.

Spatial learning in the water maze is thought to rely both on distal cues and vestibular information [Aggleton JP, Vann SD, Oswald CJP, Good M. Identifying cortical inputs to the rat hippocampus that subserves allocentric spatial processes: a simple problem with a complex answer. Hippocampus 2000;10:466-74; Pearce JM. Animal learning and cognition: an introduction. UK: Psychology Press; 1997]. Experiment 1 demonstrates that while water maze retention relies primarily on cue-platform based associations, this strategy is not precise, as animals tend to focus at the side of the pool. In experiment 2, we demonstrate that vestibular rotation eliminates this inaccuracy. These experiments highlight the importance of both cue and vestibular information for accurate retention of the water maze.

Analysis of Variance↗
PubMed1996

Effects of social isolation rearing on learning in the Morris water maze.

Impaired learning has been shown as a consequence of isolation-rearing in a variety of paradigms. However, there are situations in which learning in isolation-reared rats is enhanced or unimpaired compared to socially reared rats. The present experiments investigated the effects of isolation rearing on place navigation in the Morris water maze. Two complementary paradigms were studied: isolation and socially reared rats were exposed to the water maze either without drug pretreatment or following systemic administration of scopolamine. Two conditions were examined: place learning and reversal learning. Male Lister hooded rats were either housed singly (isolation reared) or in groups of four (social reared) from weaning at 21 days of age. Six weeks later place learning and reversal learning were determined using the Morris water maze. The time taken to locate the submerged island (escape latency) was used as the measure of learning ability. The results showed that place learning, and reversal learning were enhanced in isolation reared rats compared to socially reared controls. Pretreatment with scopolamine (0.3 and 0.5 mg/kg, i.p.) produced a dose-related cognitive deficit as shown by an increase in the escape latency. Scopolamine (0.3 mg/kg) impaired both place and reversal learning but this was less pronounced in isolation compared to socially-reared rats. These results suggest that rearing in isolation may enhance spatial learning though central cholinergic mechanisms.

Animals↗
PubMed2006

Neuropsychological characteristics of adolescent boys differing in risk for high blood pressure.

BACKGROUND: Individuals with established hypertension have been found to display deficits in a number of neuropsychological abilities. In general, these are probably due to structural changes in the brain produced by sustained high blood pressure. However, a potentially important line of research suggests that some of these deficits may extend to younger individuals with less severe elevations of blood pressure, perhaps even children, and thus be related more to risk for hypertension than hypertension per se. PURPOSE: The objective was to examine the relationships between neuropsychological function and risk for hypertension in children. METHODS: Measurements of blood pressure and parental history of hypertension were obtained in 88 French-Canadian 14-year-old boys and used to predict performance on a neuropsychological battery. RESULTS: Boys at greater risk of hypertension by virtue of having a parental history of high blood pressure and normatively elevated systolic blood pressure had significantly lower scores on a verbal learning factor score compared to boys at lower risk. Boys with normatively elevated systolic blood pressure also had significantly lower scores on a spatial learning and memory factor score compared to boys with lower blood pressure. The results could not be attributed to differences in family socioeconomic status. CONCLUSIONS: Using a younger sample than typically employed in the area, the results support previous suggestions that some of the neuropsychological characteristics displayed by hypertensive individuals may predate the development of clinically elevated blood pressure and could be associated with risk for the disorder.

Adolescent↗
PubMed1998

Effects of enriched postoperative housing conditions on spatial memory deficits in rats with selective lesions of either the hippocampus, subiculum or entorhinal cortex.

Long-Evans male, adult rats received selective and bilateral lesions of either the hippocampus, subiculum or lateral entorhinal cortex, and were then housed for 30 days in either enriched or standard conditions. Rats were then tested in the eight-arm radial maze to assess spatial working memory and the strategies that were employed (i.e. pattern of arms visited). Lesions of the hippocampus induced both a working-memory impairment and a loss in the use of allocentric strategies to perform the task. Rats with lesions of the subiculum were also impaired but less than hippocampectomized rats and showed a similar pattern of arm visits as control rats. In contrast with other lesioned rats, rats with lateral entorhinal cortex lesions performed the task like control rats. Postoperative enriched housing conditions (EHC) globally enhanced performance of rats, but did not affect the strategies selected by the rats to solve the task. The beneficial effect of EHC was particularly obvious in rats with lesions of the subiculum. In enriched rats with such lesions, performance was not significantly different from that of control rats housed in standard conditions. The present results indicate that 1) the structures within the hippocampal formation are not similarly involved in spatial learning and memory processes and in the management of navigational demands of the radial maze, and 2) enriched conditions may enhance the spared spatial abilities of some lesioned rats thus promoting functional recovery.

Journal Article↗
PubMed2006

Altered navigational strategy use and visuospatial deficits in hAPP transgenic mice.

Navigation deficits are prominent in Alzheimer's disease (AD) patients and transgenic mice expressing familial AD-mutant hAPP and A beta peptides. To determine the impact of strategy use on these deficits, we assessed hAPP and nontransgenic mice in a cross maze that can be solved by allocentric (world-based) or egocentric (self-based) strategies. Most nontransgenic mice used allocentric strategies, whereas half of hAPP mice were egocentric. At 3 months, all mice learned the cross maze rapidly; at 6 months, only allocentric hAPP mice were impaired. At 3 and 6 months, hAPP mice had reduced hippocampal Fos expression, which correlated with cross maze learning in older mice. Striatal pCREB expression was unaltered in hAPP mice, suggesting striatal sparing. We conclude that egocentric strategy use may be an earlier indicator of hAPP/A beta-induced hippocampal impairment than spatial learning deficits. Persistent use of allocentric strategies when egocentric strategies are available is maladaptive when there is hippocampal damage. Interventions promoting flexibility in selecting learning strategies might help circumvent otherwise debilitating navigational deficits caused by AD-related hippocampal dysfunction.

Amyloid beta-Peptides↗