Studies in motivation and learning: thirsty rats trained in a maze with food but no water; then run hungry.
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Long-term effects of neonatal methamphetamine exposure in rats on spatial learning in the Barnes maze and on cliff avoidance, corticosterone release, and neurotoxicity in adulthood.
Methamphetamine (MA) is a commonly abused stimulant and because of its addictive properties, abusers may not cease use during pregnancy, thereby exposing the fetus to the drug. The consequences of such exposure remain largely unknown however data from animal models show that long-term deficits in spatial learning and memory in the Morris water maze (MWM) occur. In this study we explored the spatial learning ability of rats treated four times daily with MA (5 mg/kg/dose) during the sensitive period for induction of MWM deficits, postnatal days (P) 11-20, using a different maze. In adulthood the animals were tested in a non-swimming spatial task, the Barnes maze, using either aversive (bright light) or appetitive (food reward) motivation. Approximately 30 days after behavioral testing, the pituitary and adrenal response to forced swim was assessed and susceptibility to MA-induced neurotoxicity measured. MA-treated animals tested in the aversive, but not the appetitive, version of the Barnes maze demonstrated spatial learning deficits. An attenuated corticosterone response in MA-treated animals was observed following forced swimming, however no differences in ACTH were found. Following acute MA administration in adulthood to all animals, the neonatally MA-treated animals displayed longer latencies to fall from a cliff than neonatally saline-treated rats given the same acute MA dose. This effect supports previous data showing hypoactivity in neonatally MA-treated animals. Acute MA treatment caused comparable striatal monoamine depletions in all groups, although females treated with MA as neonates displayed increased basal levels of corticosterone three days after the acute dose. These data demonstrate that MA administration during the neonatal period impairs spatial learning in an aversive non-swimming task and alters the adrenal response to a forced swim stressor, suggesting that the adrenal output during learning may contribute to the spatial learning deficits.
Adrenal Glands↗
[Effects of ibotenic acid lesions to rat's hippocampus CA1 on place and cue learning in Morris water maze].
It is known that the multiple injections of ibotenic acid to the hippocampal CA1 (Cornu Ammonis 1) field of a rat cause cell loss and spatial learning impairment in the place task of Morris water maze. However, no study seems to have been conducted concerning the cue task of the maze. This study examined (1) whether cell loss in the CA1 field produced learning deficits in both the place and cue tasks; (2) whether training could remedy the deficit in spatial learning; and (3) whether the order of place training and cue training could change the performance outcome. Thirty-seven rats of Wistar strain were divided into Place-Cue (PC) group that received place training first and then cue training, and Cue-Place (CP) group that received training in the reverse order. Half rats in each group were damaged in the CA1 field by ibotenic acid injections. Results indicated that damage to CA1 pyramidal cells led to performance deficits only in the place task throughout training, regardless of the sequence of training. The results also indicated that training in the prior task affected learning in the succeeding task, only at the beginning of training, and the effect is transient.
Animals↗
Hippocampal synaptic depression following spatial learning in a complex maze.
Activity-dependent alteration in synaptic efficacy is referred to as synaptic plasticity and is the believed hallmark of any learning process. Here we employed a recently validated complex maze for spatial training and investigated the impact of repeated and extensive training on basal synaptic transmission of the hippocampal Schaffer collateral-CA1 synaptic connection in vitro. In the present experiments, male CD-1 mice were trained in a complex maze for eight consecutive days five times a day. Subsequently, input-output functions of field excitatory postsynaptic potentials (fEPSPs) recorded in the CA1 area following stimulation of the Schaffer collateral-commissural fiber pathway were analyzed in acute hippocampal slices. We found a marked right shift of the fEPSP response in trained compared to untrained animals while fiber volley size remained unchanged. The findings provide evidence for a direct implication of homosynaptic hippocampal long-term depression in a spatial learning paradigm.
Animals↗
Ontogenetic differences in retention of spatial learning tested with the Morris water maze.
Two experiments examined retention of spatial learning in rats using a Morris water maze. Retention was scored in terms of probe trial performance when the platform was removed. Latency to reach the platform location, percent of time in the quadrant that had contained the platform, and relative frequency of visits to the platform location were analyzed. Results of the first experiment showed that preweanlings and juveniles exhibited substantial forgetting at 3- and 7-day retention intervals. Forgetting in adults was much lower than that found in the younger animals, and no differences in amount of forgetting appeared between the 3- and 7-day retention intervals at any age. The second experiment showed that forgetting in juveniles was alleviated by a single training trial administered just prior to the probe trial. These results are discussed in terms of ontogenetic differences in memory processing and measurement issues pertinent to the Morris water maze test procedure.
Aging↗
Selective lesion of cholinergic neurons in the medial septum by 192 IgG-saporin impairs learning in a delayed matching to position T-maze paradigm.
This study examined whether selective destruction of cholinergic neurons in the medial septum impairs acquisition of a delayed matching-to-position (DMP) spatial memory task. Either the selective immunotoxin 192 IgG-saporin (SAP; 0.22 or 1.0 microg) or the non-selective excitatory neurotoxin ibotenate (IBO; 5 microg), was infused directly into the medial septum of rats. Both doses of SAP, but not IBO, significantly impaired acquisition of the DMP task and blunted the initial alternating behavior of the rats in the T-maze. Histochemical staining revealed that both doses of SAP produced a near complete depletion of choline acetyltransferase (ChAT)-positive neurons in the medial septum. Some loss of parvalbumin staining was observed following administration of the higher dose, but not the lower dose, of SAP. In contrast, IBO produced a nearly complete depletion of parvalbumin-positive staining throughout the medial septum. IBO also produced a loss of ChAT-positive neurons and considerable local damage in the medial septum around the area of injection; however, many ChAT-positive neurons in the medial septum distal to the injection remained. A significant correlation between the number of days to reach criterion and ChAT activity in the frontal cortex and hippocampus was observed. The results suggest that low doses of SAP can be used to selectively destroy cholinergic neurons in the medial septum, and that selective destruction of these neurons significantly impairs acquisition of the DMP task. We propose that acquisition of the DMP task is a sensitive behavioral assay for the selective loss of basal forebrain cholinergic projections.
Animals↗
The effects of AMPA-induced lesions of the septo-hippocampal cholinergic projection on aversive conditioning to explicit and contextual cues and spatial learning in the water maze.
The environmental context of an animal both subsumes and is associated with the explicit cues that guide its behavioural responses. Recent work in this laboratory suggests that learning about the relationship between the cues which comprise a context depends on the hippocampus. In the present study the role of the cholinergic input to the hippocampus in contextual learning was assessed in rats using a conditioned stimulus/context conditioning paradigm and spatial learning in the Morris water maze. In the former, a place preference apparatus provided the context. The subject was confined in the black chamber and a 'clicker' conditioned stimulus was presented five times in a 20 min period. A trace interval of 5 or 30 s, depending on the group, was interposed between the end of the clicker and a footshock. Theory predicts that animals in the 5 s condition will learn more about the clicker as a predictor of shock and become strongly conditioned, while those in the 30 s condition learn relatively more about the context. Conditioning to the clicker (conditioned stimulus) was measured in a separate lick suppression chamber--presentation of the clicker suppresses drinking, and contextual learning was determined by recording the time spent on the black side of the place preference apparatus when both the black and a familiar white chamber were accessible. Lesions of the medial septum/diagonal band induced by RS-alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid (AMPA) enhanced contextual learning in this paradigm but disrupted conditioned stimulus conditioning in the 30 s condition. Acquisition of the Morris water maze was largely unimpaired. The results are suggested to reflect a shift towards the use of hippocampal-dependent contextual learning strategies in lesioned animals.
Acetylcholine↗
Paradoxical effects of learning the Morris water maze on adult hippocampal neurogenesis in mice may be explained by a combination of stress and physical activity.
Studies in rats that assessed the relation of hippocampus-dependent learning and adult hippocampal neurogenesis suggested a direct regulatory effect of learning on neurogenesis, whereas a similar study in mice had not found such causal link. We here report a substantial decrease of BrdU-positive cells and other measures of adult hippocampal neurogenesis in mice trained in the hidden (HID) or cued version (VIS) of the Morris water maze as compared to untrained animals (CTR). Particularly, cells on advanced stages of neuronal development contributed to this decrease, whereas earlier progenitors (type 2 cells) were not diminished in HID, but were diminished in VIS as compared to CTR. The differential regulation of type 2 cells in HID and VIS may have been caused by a different degree of physical activity, given that a time-yoked control group did not differ from HID, and type 2 cells reportedly constitute the proliferative dentate gyrus population that primarily responds to physical activity. The decrease of hippocampal neurogenesis by water maze training was reversible by pre-exposing animals to the water maze prior to training, suggesting that stress associated with training may have caused the acute downregulation of adult neurogenesis. We propose that in mice the Morris water maze does not provide a pure enough learning stimulus to study the presumed effects of 'learning' on adult neurogenesis. In addition, however, our data show that physical activity that is intricately linked to many cognitive tasks in rodents might play an important role in explaining effects of learning on cellular hippocampal plasticity.
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Effects of injections of glucose into the dorsal striatum on learning of place and response mazes.
The present experiment tested the hypothesis that facilitation of striatal function with intra-striatal glucose injections would facilitate learning a striatum-dependent response maze and impair learning a hippocampus-dependent place maze. Food-deprived Sprague-Dawley male rats were trained to find food in a Y-maze. In the place version of the maze, rats were rewarded for learning to go to an arm located in a fixed location while in the response task rats were rewarded for consistently turning in the same direction at the choice point. Artificial cerebrospinal fluid (1 microL) containing either 0.7 nmol of glucose (control) or 20 nmol of glucose was injected bilaterally into the dorsal striatum immediately before training. The animals were trained to a criterion of 9/10 correct choices. In the place maze, glucose injections impaired learning, as measured by number of trials required to reach 9/10 correct. However, in the response task, glucose injections did not enhance learning. A subsequent experiment examined the effects of intra-striatal glucose injections on acquisition of the response task under two different visual cue conditions, addition of an intra-maze light cue that predicted the correct arm or with removal of most visual extramaze cues. Glucose again failed to facilitate acquisition of the response task under these conditions. These findings suggest that facilitation of striatal function via intra-striatal glucose injections is sufficient to impair place learning but not to enhance response learning, perhaps separating the neurochemical mechanisms for striatal involvement in impairment of place and enhancement of response learning.
Animals↗
Effects of subchronic methylphenidate hydrochloride administration on the locomotor and exploratory behavior of prepubertal mice.
The increasing use of methylphenidate hydrochloride (MPH) in children led us to examine the effects of MPH administration in developing mice. Male CD-1 mice were administered MPH (40 mg/kg, subcutaneously) or saline daily from postnatal days 26-32. The mice were then tested from postnatal days 33-37 for locomotion and exploration in the open field, anxiety in the elevated plus maze, and learning in the Morris water maze. The results indicate that MPH-pretreated mice were more exploratory and less fearful in the open field, entering more center squares than saline controls. MPH-pretreated mice also exhibited less anxiety, spending more time in the open arm and exhibiting more head dips in the elevated plus maze than controls. There was no significant difference between MPH and saline-treated mice in the time taken to find the visible or hidden platform in the water maze task. The results indicate that treatment with MPH has significant effects on later behavior, reducing fear and anxiety, and increasing exploration, but no effect on performance in a spatial learning task.
Animals↗
Learning and memory in agmatine-treated rats.
Agmatine, a noncompetitive N-methyl-D-aspartate (NMDA) antagonist, was examined for its role in water maze place learning, contextual and auditory-cued (discrete) fear learning and conditioned taste aversion learning, when administered systemically. Male Wistar rats were given saline or 1, 5, 10 or 50 mg/kg agmatine ip 20 min prior to or 30 min following daily training sessions in a hidden-platform (place learning) water maze task. Agmatine did not affect latencies to find the hidden platform or preference for the training quadrant during probe trials. When administered 20 min prior to contextual or auditory-cued fear-conditioning sessions, these doses of agmatine evoked a linear dose-dependent impairment in the magnitude of learned fear to the contextual stimuli when assessed during extinction trials 24 h later, but had no effect on the magnitude of learned fear to the auditory stimulus. Inferences of baseline motor activity and ability to respond to the presentation of footshock stimuli were not affected by the treatment. Injections of 50 mg/kg agmatine concurrently with a malaise-evoking agent following presentations to a novel sucrose solution abolished learned taste aversions; this agent did not evoke conditioned taste aversions alone. These studies indicate that systemically administered agmatine selectively impairs behavioral inferences of specific types of learning and memory.
Agmatine↗
[The discriminative stimulus properties of naloxone during dissociative learning in a Y maze in morphine-dependent rats].
The study was dedicated to evaluation of discriminative stimulus properties of opiate withdrawal syndrome precipitated by naloxon. The possibility of naloxon-appropriate reaction significantly increased in a dose-dependent manner (0-1.0 mg/kg, ED50 = 0.03 mg/kg) and was observed during the period of morphine withdrawal (8-96 h, peak at 24 h). Naloxone stimulus effects were antagonized by morphine (10-100.mg/kg), thus providing the experimental evidence for competitive and saturatable nature of interaction with opiate receptors. The probability of naloxone-appropriate reaction decreased during administration of the conditioned stimulus associated with morphine injection. Ligands of peripheral opiate receptors failed to either substitute for naloxone (methylnaloxon, 0.1-3.0 mg/kg) or attenuate naloxone stimulus effects (loperamide, 1-30 mg/kg).
Animals↗
Are glutamate receptors specifically implicated in some forms of memory processes?
Convergent data indicate that certain substances that interact with N-methyl-D-aspartate (NMDA) receptors or metabotropic glutamate receptors (mGluRs) do not affect acquisition processes per se, or retrieval, but interfere specifically with the formation of memory traces. This action differs widely in its amplitude and time-course according to the learning task used. We showed that systemic injection of the competitive NMDA receptor antagonists, gamma-L-glutamyl-L-aspartate (gamma-LGLA) and 3-(2-carboxypiperazin-4-yl)propyl-1-phosphonate (CPP), or intracerebroventricular infusion of D-2-amino-5-phosphonovalerate (D-AP5), immediately following acquisition of a Y-maze avoidance learning task in mice, deeply impaired retention of the temporal component of the task (leaving the start alley within the first 5 s of a trial), which significantly improved in controls during the hours following acquisition. In contrast the same substances had no or only slight effects on retention of the discrimination component (choice of the correct alley), which did not improve over time in control animals. This retention deficit did not appear to be due to an action on acquisition, retrieval and/or forgetting processes, or to state-dependent effects. Moreover, gamma-LGLA, CPP or AP5, when administered immediately after partial acquisition of a food-reinforced bar-press task, suppressed the spontaneous improvement in post-training performance observed in control mice 24 h after the training session. (R,S)-alpha-methyl-4-carboxyphenylglycine (MCPG), an antagonist of mGluRs, also suppressed the post-training performance increment and its effects were antagonized by the co-administration of trans-ACPD, an agonist of mGluRs. Post-training improvement of performance over time is thought to reflect an active and dynamic process, leading to the organization of memory traces. According to this hypothesis, our results suggest that synaptic plasticity mediated by NMDA receptors and/or mGluRs activation is involved in mechanisms underlying long-term consolidation of memory traces.
Animals↗
Validation of a radial maze test for assessing learning and memory in rats.
Choice behavior of rats in a radially symmetrical 6-arm maze, without food reward, was validated for assessing changes in learning and memory following treatment with 4 psychoactive agents. The test is designed for future use in routine toxicity studies with laboratory rodents. Each radial main arm of the maze leads to a T-shaped choice-point with a blind alley on the left and a long angled alley on the right. Order of choice of the radial main arms served to score within-session working memory, by evaluating relative recency of arm reentries. The choice between blind alley and long-angled alley at the T-intersections provided a measure of between-session reference memory. Maze behavior as an indicator for impairment in learning and memory was validated by testing rats treated with d-amphetamine, chlorpromazine, scopolamine and physostigmine. Based on the above evaluations, working memory was found to be severely impaired by 0.3 and 1.0 mg/kg scopolamine, and reference memory to be improved by 0.02 mg/kg physostigmine and 1.0 mg/kg amphetamine. Locomotor activity, in terms of the total number of arm choices per test session, was altered by all substances as expected from previous reports in the literature. The test appears to be a valid and sensitive method for assessing learning and memory in the rat without the use of food reward, and thus well suited for implementation in routine toxicity studies with rodents.
Animals↗
[A simple multiple maze test to estimate learning and memory in mice: application to the effect of scopolamine on learning and memory].
The apparatus consists of a home cage, a maze cage and a starting box. A maze with four right-middle-left decisions was placed in the maze cage. The starting box was attached and a water tap was placed at an area corresponding to the entrance of the maze. The exit of the maze and the home cage are connected with a tunnel. Food was placed in the home cage. 1) Mice were housed for 10 hr a day in the apparatus and then removed to another cage for fasting. One trial a day was carried out after fasting for more than 12 hr. In each trial, a mouse was put at the starting box, and then the number of errors (entering a blind alley) and the time until the mouse reached the home cage were counted. The mouse passed through the maze with a small number of errors and time. 2) Administration of scopolamine (0.125-0.5 mg/kg, i.p.) to a mouse that had mastered the maze transiently disturbed the maze performance dose-dependently. 3) Mice were housed for 4 hr a day. Scopolamine (0.25 mg/kg, i.p.) was administered either before or after the housing. Scopolamine disturbed the maze performance in the case of both procedures. These results suggest that the method is useful for estimating the memory in mice.
Animals↗
Phencyclidine and behavior: II. Active avoidance learning and radial arm maze performance.
Rats with injections of 4 or 8 mg/kg of phencyclidine (PCP) are impaired in the acquisition of active avoidance learning and radial arm maze performance. This impairment was not due to a change in detectability of aversive stimuli or the inability to perform the correct response. The primary deficit appears to be the inability of PCP injected animals to encode the appropriate attributes (e.g., environmental context, response selection, and emotion) associated with each task.
Animals↗
Comparison of the effects of the 5-HT3 receptor antagonists WAY-100579 and ondansetron on spatial learning in the water maze in rats with excitotoxic lesions of the forebrain cholinergic projection system.
The effects of the 5-HT3 receptor antagonists. WAY-100,579 and ondansetron (both at doses of 0.001, 0.01 and 0.1 mg/kg s.c.) and the muscarinic receptor agonist arecoline (1.0 mg/kg s.c.), on spatial learning and memory in the water maze were examined in rats after combined S-AMPA lesions to the nucleus basalis and medial septal brain regions. Lesioned rats showed substantially increased latency to find the submerged platform, and spent less time searching in the correct quadrant, and more time circling the periphery of the pool, relative to controls. Lesioned rats treated with WAY-100,579, ondansetron and arecoline exhibited marked improvement in these parameters of learning relative to lesioned animals, with arecoline-treated animals showing the most substantial recovery. Linear dose-related trends of improvement were seen with both of the 5-HT3 antagonists. In probe trials, testing retention of the platform position 24 and 72 h after the end of training, control rats exhibited substantial superiority relative to lesioned rats in accuracy of search in the training quadrant and former platform area, matched by rats treated with arecoline on the first, and by rats treated with the two higher doses of WAY-100,579 and ondansetron on the second probe trial. These results are consistent with our previous studies which demonstrated that another selective 5-HT3 receptor antagonist. WAY-100,289, significantly reversed the cognitive deficits in water maze performance induced by ibotenic acid lesions of forebrain cholinergic projection system. Therefore, selective 5-HT3 receptor antagonists may provide a novel effective therapy for treating cognitive deficits associated with degeneration of central cholinergic neurones, such as Alzheimer's disease or age-associated memory impairment.
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Posttraining paradoxical sleep in rats is increased after spatial learning in the Morris water maze.
The role of posttraining paradoxical sleep (PS) in spatial or nonspatial learning in the Morris water maze was evaluated. Sprague-Dawley rats were given a 12-trial training session in either the hidden or the visible platform versions of the task. Subgroups then underwent paradoxical sleep deprivation (PSD) beginning at different times after training. Rats with PSD imposed from 1-4 hr after spatial training had poorer retest scores than any other group. Other rats, implanted with electrodes to permit continuous recording of sleep electroencephalography, were found to undergo a prolonged period of elevated PS after spatial training. By contrast, rats trained in the nonspatial version of the water maze task did not show retention deficits after PSD or elevated PS after training. These results support a role for PS in spatial, but not nonspatial, learning in the Morris water maze.
Animals↗