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PubMed2001

Spatial learning deficits without hippocampal neuronal loss in a model of early-onset epilepsy.

Studies were undertaken to examine the effects recurrent early-life seizures have on the ability of rats to acquire spatial memories in adulthood. A minute quantity of tetanus toxin was injected unilaterally into the hippocampus on postnatal day 10. Within 48 h, rats developed recurrent seizures that persisted for 1 week. Between postnatal days 57 and 61, rats were trained in a Morris water maze. Toxin-injected rats were markedly deficient in learning this task. While these rats showed gradual improvement in escape latencies over 20 trials, their performance always lagged behind that of controls. Poor performance could not be explained by motor impairments or motivational difficulties since swimming speed was similar for the groups. Only eight of 16 toxin-injected animals showed focal interictal spikes in the hippocampus during electroencephalographic recordings. This suggests that learning deficiencies and chronic epilepsy may be independent products of recurrent early-life seizures. A quantitative analysis of hippocampus revealed a significant decrease in neuronal density in stratum pyramidale of experimental rats. However, the differences were largely explained by a concomitant increase in the area of stratum pyramidale. Studies of glial fibrillary acidic protein expression and spread of horseradish peroxidase-conjugated tetanus toxin in the hippocampus suggest that the dispersion of cell bodies in stratum pyramidale can neither be explained by a reactive gliosis nor the direct action of the toxin itself. Taken together, we suggest that recurrent seizures beginning in early life can lead to a significant deficiency in spatial learning without ongoing hippocampal synchronized network discharging or a substantial loss of hippocampal pyramidal cells.

Action Potentials↗
PubMed2000

Nonreceptor tyrosine protein kinase pp60c-src in spatial learning: synapse-specific changes in its gene expression, tyrosine phosphorylation, and protein-protein interactions.

c-src is a nonreceptor tyrosine protein kinase that is highly concentrated in synaptic regions, including synaptic vesicles and growth cones. Here, we report that the mRNA signal of pp60c-src is widely distributed in the rat brain with particularly high concentrations in the hippocampus. After spatial maze learning, up-regulation of c-src mRNA was observed in the CA3 region of the hippocampus, which was accompanied by increases in pp60c-src protein in hippocampal synaptosomal preparations. Training also triggered an increase in c-src protein tyrosine kinase activity that was correlated with its tyrosine dephosphorylation in the synaptic membrane fraction. After training, pp60c-src from hippocampus showed enhanced interactions with synaptic proteins such as synapsin I, synaptophysin, and the type 2 N-methyl-d-aspartate receptor, as well as the cytoskeletal protein actin. The association of pp60c-src with insulin receptor in the synaptic membrane fraction, however, was temporally decreased after training. Furthermore, in vitro results showed that Ca(2+) and protein kinase C might be involved in the regulation of protein-protein interactions of pp60c-src. These results suggest, therefore, that pp60c-src participates in the regulation of hippocampal synaptic activity during learning and memory.

Animals↗
PubMed1986

Scopolamine-induced deficits in acquisition of a complex spatial learning.

The role of scopolamine was studied in a complex spatial orientation task. The procedure involved an increasing difficulty of the task: at the pretraining stage a cue (box) was placed at the reinforcement spot and the animal could give a correct response by adopting either a cue-strategy or an orientation response (i.e., go to the arm on the right of a visual landmark). In the subsequent spatial training, the box was removed, so that the orientation response was the only correct one. Results show that scopolamine-injected animals are able to use a cue-strategy but are unable to acquire a spatial orientation strategy: this more complex task asks for more time and for more sustained attention. When the response is already partly acquired, scopolamine has less effect. The cholinergic system would thus be involved in the quality or even the complexity of the response rather than in the retention itself. Though a state-dependent effect may not be excluded, it by itself cannot explain the observed differences. Finally, an impairment of the maintenance of attention could be responsible for the deficits observed in the acquisition of the complex task.

Animals↗
PubMed1989

Early rearing environment and dorsal hippocampal ibotenic acid lesions: long-term influences on spatial learning and alternation in the rat.

Behavioural responses in a set of spatial and cue tasks were assessed in adult rats that had been given ibotenic acid lesions of the dorsal hippocampus at weaning. The lesions or sham operations were immediately followed by one month of differential rearing, either in enriched, social or isolated housing environments. The differential rearing was followed by standard (social) housing conditions until behavioural testing began at 4 months of age. Compared to sham-operated rats, the rats with early cytotoxic lesions showed substantial impairments on learning and efficient strategy formation in radial arm maze, retention of a spatial location, but not of a cue-marked location, in a + maze and spontaneous alternation. Differential rearing had some long-term effects depending on the task. Sham-operated rats which had been housed in isolation used a pattern of strategies in the radial arm maze that resembled the pattern used by rats with lesions. Early enrichment, on the other hand, alleviated lesion deficits only in a spontaneous alternation task in a T-maze where the variety and salience of proximal cues were maximised. Enrichment increased lesion deficits in the radial maze task, where distal cues only could guide performance. The results suggest that the hippocampus may play an important role in the use of contextual information and that behavioural recovery after early hippocampal damage--limited to situations in which featural information is highly salient--may be permanently induced by rearing in environments, as in enriched ones, where rats can attend to and manipulate environmental cues.

Animals↗
PubMed1995

Dentate gyrus destruction and spatial learning impairment after corticosteroid removal in young and middle-aged rats.

We investigated the functional and behavioral implications of chronic corticosteroid removal in young and middle-aged rats. Prepubertal and 13-month-old rats were adrenalectomized (ADX) or sham operated (SHAM). The young ADX rats were divided further into three groups: ADX with no hormone replacement, ADX given corticosterone chronically, (chCORT), and ADX given corticosterone acutely at the time of Morris water maze testing (acCORT). All rats were run on the Morris water maze 12 weeks after surgery. They were then sacrificed and the brains were removed for histological analysis. The results showed that prolonged corticosteroid absence caused major damage to the dentate gyrus and learning impairment on the Morris water maze. The chCORT rats had little dentate gyrus cell loss and were as efficient as the controls in Morris water maze performance, whereas the acCORT rats had dentate gyrus cell loss and were impaired in the spatial acquisition task. Furthermore, exogenously administered corticosterone had an interactive effect on ADX rats. Water maze performance was improved in dentate gyrus damaged rats (acCORT) compared to ADX rats not given corticosterone, whereas ADX rats with very little dentate gyrus damage (chCORT) did not exhibit better water maze performance relative to controls. Middle-aged ADX rats lost cells only in the dorsal blade of the dentate gyrus but they did not show a learning impairment in the Morris water maze relative to the middle-aged controls. These results indicate that corticosteroids are trophic for the dentate gyrus, that mature granule cells are less affected by adrenalectomy, that corticosteroid absence is responsible for some water maze impairment in ADX rats, but that in addition to corticosteroid absence, a substantial amount of dentate gyrus damage is necessary to impair spatial learning.

Adrenal Cortex Hormones↗
PubMedDate not supplied

Effect of sex and age on brain monoamines and spatial learning in rats.

The concentrations of noradrenaline (NA), dopamine (DA), serotonin (5-HT), and their metabolites were measured in the prefrontal cortex, caudate-putamen, and hippocampus in young (3 months) and aged (27-31 months) Wistar rats of both sexes. Age-related changes were found in prefrontal NA and HVA/DA ratio, striatal DA and DOPAC/DA ratio, and striatal and hippocampal 5-HT and 5-HIAA/5-HT ratio. Age and sex dependent changes were found in striatal DA and DOPAC/DA ratio, and hippocampal MHPG-SO4/NA ratio. The aged rats were tested in spatial discrimination and reversal tasks in a T maze. The effects of alpha 2-agonist medetomidine (3 micrograms/kg) on the task performance were assessed in relation to individual variation in monoamine metabolism. Medetomidine impaired spatial discrimination learning of the aged rats by interacting with the hippocampal 5-HT turnover. Medetomidine improved reversal learning through an interaction with the striatal DA turnover and reduced the number of perseverative errors after reversal, mainly due to its interaction with the prefrontal NA turnover. It is concluded that the memory enhancing effect of drugs acting through the brain monoamine systems is highly dependent on the stage of degeneration of these systems that show considerable individual variation in aged animals.

Adrenergic alpha-Agonists↗
PubMed1990

The effect of early experience on water maze spatial learning and memory in rats.

In the first of two experiments on spatial competence, groups of light-reared (LR) and dark-reared (DR) rats were compared using a "latent learning" variation of the Morris Water Maze task. On their initial test, the LR rats benefited more than DR rats did from viewing the room/pool from a platform in the correct location. Further, visually experienced rats remember the location of the platform more than DR rats when retested one month later. In a second experiment, in which a proximal cue as well as location was varied from trial to trial. LR rats again proved to be more competent than their DR counterparts. This second task also revealed significant benefits related to stimulation history in the case of a third group of animals raised in enriched or complex environment (CR) conditions. The results are discussed in terms of the nature of the impact of early experience on the ability to acquire and remember spatial concepts.

Animals↗
PubMed1996

Spatial learning in deer mice: sex differences and the effects of endogenous opioids and 60 Hz magnetic fields.

We examined the effects of brief exposure to weak 60 Hz extremely low frequency (ELF) magnetic fields and opioid systems on spatial behavior and learning in reproductive adult male and female deer mice, Peromyscus maniculatus. Sex differences were evident in spatial performance, with male deer mice displaying significantly better performance than female mice in the Morris water maze, whereby animals had to acquire and retain the location of a submerged hidden platform. Brief (maximum 5 min) exposure to weak (100 microT) 60 Hz magnetic fields during task acquisition significantly improved female performance, eliminating the sex differences in acquisition. The opiate antagonist, naltrexone, also improved female acquisition, though significantly less than the magnetic fields. These facilitatory effects involved alterations of "non-spatial" (task familiarization and reduction of related anxiety/aversive related behaviors) and possibly "spatial" aspects of the task. Enhancement of enkephalin activity with the enkephalinase inhibitor, SCH 34826, significantly reduced task performance by male deer mice. Both naltrexone and the 60 Hz magnetic fields attenuated the enkephalin mediated reductions of spatial performance. These findings indicate that brief exposure to 60 Hz magnetic fields can enhance water maze task acquisition by deer mice and suggest that these facilitatory effects on spatial performance involve alterations in opioid activity.

Analgesics↗
PubMed1999

Spatial learning deficit after NMDA receptor blockade and state-dependency.

The non-competitive N-methyl-D-aspartate (NMDA) receptor antagonist dizocilpine (MK-801) (0.08 and 0.12 mg/kg, i.p.) was used to examine whether spatial memory is learned state-dependently. Rats pre-treated with drug or saline were trained for 9 days in an eight-arm radial maze, in which four arms were baited. On the tenth day MK-801-treated rats were injected with saline and one group of saline-treated rats were injected with MK-801 (0.12 mg/kg) while another received saline. Performance of spatial memory was analysed for state-dependency. Neither rats treated with 0.08 mg/kg nor 0.12 mg/kg of MK-801 for 9 days were impaired in recall of spatial memory under saline. However, MK-801 impaired acquisition of spatial memory, with deficits in working memory and less marked deficits in reference memory. Motor activity (speed) was enhanced at both doses. Thus, learning under NMDA receptor blockade does not necessarily produce a condition that impedes the expression of the learning task under a different condition.

Animals↗
PubMed1991

Spatial learning of adult rats with fetal alcohol exposure: deficits are sex-dependent.

The effects of prenatal alcohol exposure on learning in adult offspring were studied in a spatial task in a T-maze. Male and female Long-Evans rats were selected from litters whose dams had received one of three treatments: alcohol in a liquid diet (35% ethanol-derived calories, 35% EDC), pair-fed nutritional control (0% ethanol-derived calories, 0% EDC) or standard control (lab chow, LC). The task included trial-independent (reference memory) and trial-dependent (working memory) components: subjects were required to make a fixed left-right discrimination, and then to alternate left and right choices to escape water. Prenatal alcohol exposure was associated with a greater number of reference errors for both sexes; only males from the alcohol prenatal treatment group, however, were impaired on the working memory component. These results suggest that prenatal exposure to alcohol can cause behavioral dysfunctions that persist into adulthood. Secondly, the pattern of memory impairments suggests that both sexes may be equivalently damaged in neural areas subserving reference memory, but that males are selectively more vulnerable in neural areas subserving working memory.

Animals↗
PubMed1995

The effects of AMPA-induced lesions of the medial septum and vertical limb nucleus of the diagonal band of Broca on spatial delayed non-matching to sample and spatial learning in the water maze.

These experiments investigated in the rat the impact on spatial delayed non-matching to sample and on acquisition of the Morris water maze of (i) AMPA-induced lesions of the medial septal nucleus, which produced a marked reduction of hippocampal choline acetyltransferase activity and acetylcholine levels (measured using in vivo dialysis) together with lesser reductions in cholinergic markers in the cingulate cortex and (ii) similar AMPA-induced lesions of the vertical limb nucleus of the diagonal band of Broca (vDB), which produced more marked reductions in cholinergic markers in the cingulate cortex than in the hippocampus. Medial septal lesions produced a delay-dependent deficit in spatial working memory, while lesions of the vDB resulted in a delay-independent performance deficit. In addition, rats with vDB lesions adopted biased response strategies during the imposition of long delays. Neither lesion significantly affected the acquisition of a spatial reference memory task, the Morris water maze. The results are discussed in terms of cholinergic- and GABAergic-dependent functions of the hippocampal formation and cingulate cortex in spatial short-term and reference memory.

Acetylcholine↗
PubMedDate not supplied

Spatial learning on the Morris Water Maze Test after a short-term paradoxical sleep deprivation in the rat.

Twelve rats were deprived of paradoxical sleep (PS) for eight hours using the small platform method. PS-deprived and control rats then learned either the standard allocentric version (using external cues) of the Morris Water Maze (MWM) or a delayed alternation version (changing the platform location between trials: MWM(DA)). Overall, rats learning the MWM(DA) made more quadrant entries than rats learning the allocentric version. Compared to other rats, PS-deprived rats crossed more quadrants only in the MWM(DA). These results show that MWM(DA) is a more complex task to learn and is more vulnerable to PS deprivation than allocentric spatial orientation. Since delayed alternation is dependent upon frontal structures, we propose that tasks involving the frontal cortex are more sensitive to short-term PS deprivation than tasks related to hippocampal structures.

Animals↗
PubMed1998

A 2-year longitudinal study of swimming navigation in mice devoid of the prion protein: no evidence for neurological anomalies or spatial learning impairments.

Uncontrolled accumulation of a conformationally distorted protein (PrP(Sc)) is supposed to be the pathological process leading to spongiform encephalopathy. Targeted disruptions of the Prn-P gene in the mouse have resulted in animals that did not show anomalies in spatial and avoidance learning and were resistant to experimental infections. However, another Prn-P knockout mouse was reported to show ataxia and Purkinje cell degeneration developing after 70 weeks of age. In this study the initial observations are confirmed on swimming navigation of PrP-null mutant mice using an enlarged sample of 58 mice. A representative subsample of 16 mice was then followed up for their ability of swimming navigation up to an age of two years (104 weeks). Surviving PrP-null mutants (n = 4) and controls (n = 6) did not differ in any measure, nor were there indications of ataxia and Purkinje cell degeneration. It was concluded that the PrP-knockout mice used by Büeler et al. were probably normal with respect to aging processes and that resistance to scrapie is not necessarily paid for by late neuronal degeneration. The reasons for the discrepancy between different knockout experiments require experimental clarification, however.

Animals↗
PubMed2004

Pretraining or previous non-spatial experience improves spatial learning in the Morris water maze of nucleus basalis lesioned rats.

Previous experiments have shown that infusions of ibotenic acid in the nucleus basalis magnocellularis (NBM) induce a strong impairment in spatial navigation for a hidden platform in the Morris water maze. This effect was initially attributed to a cholinergic deficit, but later studies showed that performance level did not correlate with the degree of cholinergic denervation. Therefore, this impairment is due to a combined cholinergic and non-cholinergic deficit. However, it is not clear in which particular processes the NBM is involved. In this study we have evaluated the origin of behavioural impairment in spatial navigation in the water maze after an ibotenic acid-induced lesion of NBM. In the first experiment, Wistar rats were trained preoperatively in an allocentric navigation task. Postoperatively, they were tested in the same task. All lesioned animals showed a performance level similar to controls. Lesions did not impede the acquisition of new positions in the water maze, nor did affect the ability of animals to remember new platform positions after an intertrial interval of 20s, even if animals had received only allocentric experience with the platform position, or allocentric and path integration information concurrently. Lesions also failed to affect the ability to locate a hidden platform in a new environment. However, hippocampal infusions of scopolamine (5 microg) produced a severe impairment in NBM-damaged animals, without impairing performance of controls. In the second experiment Wistar rats with the same lesion were first trained in a visual-guided task in the water maze, and subsequently evaluated in the spatial task. In both tasks lesioned animals were not different from controls. These results suggest that the NBM played an important role during acquisition phases but not in the execution of spatial navigation. Moreover, the excessive emotional response displayed by lesioned animals is postulated as a relevant cause for the impairment observed in spatial navigation after NBM damage.

Animals↗
PubMed2002

[Interactive effect of MK-801 and pre-training on spatial learning in rats].

In experiment 1, the effect of an NMDA receptor antagonist, MK-801, on the formation of the spatial representation was investigated. The administration of 0.1 mg/kg of MK-801 induced learning deficits in rats (n = 10) with the Morris watermaze task. However, when rats (n = 10) were pre-trained in the same task without drug treatment, and then trained in the same task in a different environment under the influence of the same amount of the drug, their performance was not impaired. The result suggests that rats treated with MK-801 can acquire a spatial representation of their environment, and that the impairment shown by the drug-treated rats without pre-training may be due to the impairment in the learning of the problem-solving strategy required for the watermaze place task. Experiment 2 examined this possibility. Rats (n = 10) were pre-trained with a visual cue discrimination task without drug treatment and then trained in the place task with MK-801 (0.1 mg/kg) treatment. They did not show impairment in the place task, indicating that rats treated with MK-801 can learn a new problem-solving strategy. Thus the learning deficits of MK-801-treated rats that have not been pre-trained do not seem to be due to impaired acquisition of the spatial representation or of the learning of strategy required to solve the watermaze place task.

Animals↗
PubMedDate not supplied

Overexpression of a calcium-binding protein, S100 beta, in astrocytes alters synaptic plasticity and impairs spatial learning in transgenic mice.

Recent evidence suggests that slowly propagating Ca2+ waves from astrocytes can modulate the function of neurons. Altering astrocytic calcium processes in vivo may therefore affect neuronal and behavioral phenotypes. Previously, we generated transgenic mice that overexpress an astrocytic calcium-binding protein, S100 beta. Immunocytochemistry and in situ hybridization showed elevated expression in the astrocytes of the hippocampus and other brain regions. Neurons in the hippocampus were negative for S100 beta. In this paper we analyze the hippocampal electrophysiology and learning properties of mice from two transgenic lines. Significant differences were found between the hippocampal slices of normal and transgenic mice in their response to high frequency (100 Hz) stimulation. The overall distribution of post-tetanic excitatory postsynaptic potentials (EPSP) of the slices from the transgenic mice was shifted significantly toward smaller values to a degree that 25% of slices exhibited depression. The altered hippocampal neurophysiology was accompanied by an impairment in a hippocampal-dependent learning task. Transgenic mice showed significant impairment in a spatial version of the Morris water maze, however, they performed normally in non-spatial tasks. Probe trials showed that transgenic mice, though significantly impaired, also acquired spatial information. The results suggested that the impairment was not due to motor dysfunction, impaired vision or motivation of the transgenic mice, findings compatible with a possible hippocampal mechanism. We conclude that overexpression of S100 beta in astrocytes impairs, but does not abolish, the ability to solve a spatial task, and it leads to a significantly decreased post-tetanic potentiation in the hippocampal slice. We hypothesize that the changes are due to calcium mediated processes. Our results support the notion that astrocytes are involved in higher brain functions.

Animals↗
PubMed2002

Place and matching-to-place spatial learning affected by rat inbreeding (Dark-Agouti, Fischer 344) and albinism (Wistar, Sprague-Dawley) but not domestication (wild rat vs. Long-Evans, Fischer-Norway).

Domestication has been shown to produce a shift in both morphological and behavioral characteristics of animals. While changes in body weight, brain size, reproductive rates, and temperament are well documented, the effects of domestication on learning and memory are not as clearly understood. This issue is of particular importance to the use of rodent models in learning and memory where the domestication of Rattus norvegicus for research has resulted in the availability of numerous strains. To investigate cognitive effects resulting frm domestication, we examined the spatial performance of a number of rat strains: wild, Long-Evans, Fischer-Norway, Dark-Agouti, Wistar, Fischer 344, Sprague-Dawley. The wild rats served as a baseline for comparing inbred and outbred domestic strains and pigmented and albino domestic strains. Place (a measure of nonspatial and procedural learning), matching-to-place (spatial working memory), and probe (retention) performance were measured in the Morris swimming pool task. The task is an ideal means for comparing different rat strains because place learning has not been selected for in the domestication of Rattus norvegicus and because the task is ethologically relevant. The results indicated that wild rats and Long-Evans rats did not differ on any measure, with Fischer-Norway rats being only slightly inferior. Larger impairments were found in Wistar > Fischer 344 > Dark-Agouti > Sprague-Dawley strains. Impairments were more obvious on place acquisition but also occurred in matching-to-place performance. Platform crosses, but not quadrant preference was found to be correlated with place learning. In general, although nonspatial and spatial deficits were associated with both inbreeding and albinism, impaired spatial performance is not a necessary result of domestication.

Animals↗
PubMed1991

Effect of exposure to high pressure on subsequent spatial learning and memory in rats.

The effects of high helium pressure on the subsequent acquisition of spatial memory were studied in male rats. Thirty-two rats were exposed to 65 ATA helium-oxygen pressure for 4.2 days, decompressed (total time in chamber 5 days), and then tested in an eight-arm radial maze. Thirty-two control rats were exposed in the chamber to 1 ATA air. Each rat had 20 sessions in the maze (2 sessions/day for 10 days), and the number of correct (visiting an arm not previously visited to obtain the reward pellet) and incorrect choices (visiting a previously visited arm) were recorded. Statistical analysis showed that the rats exposed to 65 ATA performed significantly better than 1-ATA controls during the first 8 of 20 sessions. This effect was most pronounced in sessions 5-8. Results for sessions 9-20 showed that the pressure-treated rats still made more correct choices but to an extent that did not always reach statistical significance. Possible explanations include the pressure-treated rats performing better because of hunger after a lower food consumption at pressure. Alternatively, pressure itself may enhance proposed mechanisms of spatial memory such as long-term potentiation.

Animals↗