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PubMed1999

Hippocampectomized rats are capable of homing by path integration.

Navigation in rodents is mediated by at least 3 mechanisms: guidance, path integration, and landmark learning. The hippocampus is necessary for spatial learning based on distal landmarks, and it has been suggested that the hippocampal formation performs a form of path integration in updating place cell firing; however, the necessity of the hippocampus for path integration has not been clearly established. Rats with extensive neurotoxin lesions of the hippocampus and control rats were trained on 2 tasks in which they were required to move in total darkness from one location to another and then return to the start point. Hippocampal and control rats both used path integration in solving these tasks and did not differ in terms of the distributions of their arrival points on the return paths. We conclude that neuronal circuits sufficient for computing a homing vector using path integration are located outside the hippocampus.

Animals↗
PubMed2004

Reduced G protein-coupled signaling efficiency in retinal rod outer segments in response to n-3 fatty acid deficiency.

The fatty acid (FA) docosahexaenoic acid (DHA, 22: 6n-3) is highly enriched in membrane phospholipids of the central nervous system and retina. Loss of DHA because of n-3 FA deficiency leads to suboptimal function in learning, memory, olfactory-based discrimination, spatial learning, and visual acuity. G protein-coupled receptor (GPCR) signal transduction is a common signaling motif in these neuronal pathways. Here we investigated the effect of n-3 FA deficiency on GPCR signaling in retinal rod outer segment (ROS) membranes isolated from rats raised on n-3-adequate or -deficient diets. ROS membranes of second generation n-3 FA-deficient rats had approximately 80% less DHA than n-3-adequate rats. DHA was replaced by docosapentaenoic acid (22:5n-6), an n-6 FA. This replacement correlated with desensitization of visual signaling in n-3 FA-deficient ROS, as evidenced by reduced rhodopsin activation, rhodopsin-transducin (G(t)) coupling, cGMP phosphodiesterase activity, and slower formation of metarhodopsin II (MII) and the MII-G(t) complex relative to n-3 FA-adequate ROS. ROS membranes from n-3 FA-deficient rats exhibited a higher degree of phospholipid acyl chain order relative to n-3 FA-adequate rats. These findings reported here provide an explanation for the reduced amplitude and delayed response of the electroretinogram a-wave observed in n-3 FA deficiency in rodents and nonhuman primates. Because members of the GPCR family are widespread in signaling pathways in the nervous system, the effect of reduced GPCR signaling due to the loss of membrane DHA may serve as an explanation for the suboptimal neural signaling observed in n-3 FA deficiency.

Animals↗
PubMed2006

Aging-dependent alterations in synaptic plasticity and memory in mice that overexpress extracellular superoxide dismutase.

Oxidative damage caused by reactive oxygen species (ROS) has been proposed to be critically involved in several pathological manifestations of aging, including cognitive dysfunction. ROS, including superoxide, are generally considered as neurotoxic molecules whose effects can be alleviated by antioxidant enzymes. However, ROS also are known to be necessary components of the signal transduction cascades underlying normal synaptic plasticity. Therefore, we reasoned that the role that ROS and antioxidant enzymes play in modulating neuronal processes varies over the lifespan of an animal. We examined hippocampal long-term potentiation (LTP) and memory-related behavioral performance in transgenic mice overexpressing extracellular superoxide dismutase (EC-SOD) and their wild-type littermates at different ages. We found that aged EC-SOD transgenic mice exhibited enhanced hippocampal LTP, better cerebellum-dependent motor learning, and better hippocampus-dependent spatial learning compared with their wild-type littermates. We also found that EC-SOD overexpression impaired contextual learning, but the impairment was decreased in the aged transgenic mice. At the molecular level, aged EC-SOD transgenic mice had lower superoxide levels, a decrease in protein carbonyl levels, and a decrease in p38 and extracellular signal-regulated kinase 2 phosphorylation compared with aged wild-type mice. Our findings suggest that elevated levels of superoxide contribute to aging-related impairments in hippocampal LTP and memory, and that these impairments can be alleviated by overexpression of EC-SOD. We conclude that there is an age-dependent alteration in the role of superoxide in modulating synaptic plasticity and learning and memory.

Aging↗
PubMed1997

Methods for detecting long-term CNS dysfunction after prenatal exposure to neurotoxins.

Current U.S. Environmental Protection Agency regulatory guidelines for developmental neurotoxicity emphasize functional categories such as motor activity, auditory startle, and learning and memory. A single test of some simple form of learning and memory is accepted to meet the latter category. The rationale for this emphasis has been that sensitive and reliable methods for assessing complex learning and memory are either not available or are too burdensome, and that insufficient data exist to endorse one approach over another. There has been little discussion of the fact that learning and memory is not a single identifiable functional category and no single test can assess all types of learning and memory. Three methods for assessing complex learning and memory are presented that assess two different types of learning and memory, are relatively efficient to conduct, and are sensitive to several known neurobehavioral teratogens. The tests are a 9-unit multiple-T swimming maze, and the Morris and Barnes mazes. The first of these assesses sequential learning, while the latter two assess spatial learning. A description of each test is provided, along with procedures for their use, and data exemplifying effects obtained using developmental exposure to phenytoin, methamphetamine, and MDMA. It is argued that multiple tests of learning and memory are required to ascertain cognitive deficits; something no single method can accomplish. Methods for acoustic startle are also presented.

Animals↗
PubMed2003

Simultaneous spatial updating in nested environments.

When one moves, the spatial relationship between oneself and the entire world changes. Spatial updating refers to the cognitive process that computes these relationships as one moves. In two experiments, we tested whether spatial updating occurs automatically for multiple environments simultaneously. Participants turned relative to either a room or the surrounding campus buildings and then pointed to targets in both the environment in which they turned (updated environment) and the other environment (nonupdated environment). The participants automatically updated the room targets when they moved relative to the campus, but they did not update the campus targets when they moved relative to the room. Thus, automatic spatial updating depends on the nature of the environment. Implications for theories of spatial learning and the structure of human spatial representations are discussed.

Attention↗
PubMed2000

Quantification of swim patterns in the Morris water maze.

Spatial learning and memory in rodents is most often assessed in the Morris water maze. Neurobiologists have to distinguish behavioral patterns to unravel underlying neuronal systems. We analyzed swim patterns of mice videotaped before and after training with a multi-trial procedure in the water maze. In addition to traditional parameters, the animals' position in relation to trained and other possible platform locations was estimated five times per second by an image analysis system. This parameter, cumulative distance to platform, was correlated with time spent in the platform quadrant but not with latency to and crossings of the platform location. We detected a subgroup of animals with concentric patterns within the group of spatial/persistent patterns. Random patterns were classified as well. Swim patterns before training were not predictive for the one after training. In summary, image analysis systems have made it very convenient to quantify behavior. Using their capacity, we have further improved the analysis of swim patterns, revealing animals' different approaches to solve a problem.

Animals↗
PubMed1994

Spatial water maze learning using celestial cues by the meadow vole, Microtus pennsylvanicus.

The Morris water maze is widely used to evaluate to evaluate the spatial learning ability of rodents under laboratory settings. The present study demonstrates that reproductive male meadow voles, Microtus pennsylvanicus, are able to acquire and retain a spatial water maze task using celestial cues. Voles were able to acquire a modified outdoor Morris water maze task over 4 trials per day, whereby they had to learn and remember the location of a submerged hidden platform, using the position of the sun and associated celestial cues. Their proficiency on this task was related to the availability of the celestial cues, with voles displaying significantly poorer spatial navigation on overcast than clear days and when the testing time (and position of the sun and associated celestial cues) was shifted from morning to afternoon. These findings with meadow voles support the ecological relevance of the water maze task.

Animals↗
PubMed2003

Navigational place learning in children and young adults as assessed with a standardized locomotor search task.

Spatial behaviour was investigated using a spatial learning task based on the Radial Arm Maze, the Morris Water Maze, and open-field search-task procedures. Ninety-six healthy children from six age groups (3, 4, 5, 7, 10 and 12 years) with no history of CNS disorders were studied with respect to the emergence of position-, cue- and place responses. Participants were to detect x out of n hidden locations, frames of reference could be varied systematically, and three spatial memory errors and speed of navigation were recorded automatically. Task difficulties were equivalent for each age group. Results showed that navigational place learning was fully developed by the age of 10, whereas participants relied on cue orientation up to age 7. Even in the youngest group, the task could be achieved without relying on egocentric orientation, provided that proximal cues were presented. Most of the errors were of the reference memory type, whereas working memory errors were extremely rare. Speed of navigation markedly improved between age 5 and 7. An additional experiment showed that navigational place-learning behaviour was clearly dependent on distal cues. A third study showed that in young adults, learning of the spatial layout improved, but performance on the place task did not improve any further. No sex differences were observed.

Adolescent↗
PubMed2006

Deletion of the kinase domain from death-associated protein kinase enhances spatial memory in mice.

Death-associated protein kinase (DAPK) is a Ca2+/calmodulin-dependent serine/threonine kinase that is thought to mediate apoptosis. DAPK is highly expressed in hippocampal neurons which are essential elements for memory formation. To examine if DAPK is implicated in spatial learning and memory, both wild-type and DAPK-mutant mice were subjected to Morris water maze tests. DAPK-mutant mice were generated by deleting 74 amino acids from the catalytic kinase domain of DAPK, and were used to investigate roles of the DAPK kinase domain in regulating spatial memory. Both mutant and wild-type mice were able to learn the water maze tasks to locate a hidden escape platform. In the first probe test, mutant mice showed a more precise memory for platform position compared to wild-type mice. In the reversal training in which the platform was located opposite from the original position, DAPK-mutant mice exhibited superior spatial learning compared to wild-type mice. DAPK-mutant mice also showed a more precise memory than their wild-type littermates in the probe trial of reversal test. Thus, the present results revealed crucial implications of DAPK in regulating spatial memory in mice.

Animals↗
PubMed1993

Effects of ketamine and L-glutamic acid diethyl ester on spatial and nonspatial learning tasks in rats.

An NMDA antagonist, ketamine, at the highest dose tested (15 mg/kg), impaired the acquisition of a hole-board spatial learning task but not the acquisition of a left-right alternation task. A non-NMDA (quisqualate) antagonist, L-glutamic acid diethyl ester (LGDE), did not impair the acquisition of either task. Both drugs had effects on different aspects of a go-no go discrimination task and a straight runway task, ketamine tending to activate and LGDE tending to slow rats. These results concur with previous research regarding the sensitivity of some spatial tasks to NMDA antagonism. Non-NMDA antagonists affect behavior without causing spatial deficits.

Animals↗
PubMed1999

Hippocampal encoding of non-spatial trace conditioning.

Trace eyeblink classical conditioning is a non-spatial learning paradigm that requires an intact hippocampus. This task is hippocampus-dependent because the auditory tone conditioned stimulus (CS) is temporally separated from the corneal airpuff unconditioned stimulus (US) by a 500-ms trace interval. Our laboratory has performed a series of neurophysiological experiments that have examined the activity of pyramidal cells in the CA1 area of the hippocampus during trace eyeblink conditioning. We have found that the non-spatial stimuli involved in this paradigm are encoded in the hippocampus in a logical order that is necessary for their association and the subsequent expression of behavioral learning. Although there were many profiles of single neurons responding to the CS-US trial during training, the majority of the neurons showed an increase in activity to the airpuff-US. Prior to learning, it appears that hippocampal cells and ensembles of cells were preferentially attending to the stimulus with immediate behavioral importance, the US. Hippocampal cells then began to respond to the associated neutral stimulus, the CS. Shortly thereafter, animals began to show increases in the behavioral expression of CRs. In some experiments, hippocampal neurons from aged animals exhibited impairments in the encoding of CS and US information. These aged animals were not able to associate these stimuli and acquire trace eyeblink CRs. Our findings along with the findings of other spatial learning studies, suggest that the hippocampus is involved in encoding information about discontiguous sets of stimuli, either spatial or nonspatial, especially early in the learning process.

Animals↗
PubMed2001

Theta rhythm of hippocampal CA1 neuron activity: gating by GABAergic synaptic depolarization.

Information processing and memory consolidation during exploratory behavior require synchronized activity known as hippocampal theta (theta) rhythm. While it is well established that the theta activity depends on cholinergic inputs from the medial septum/vertical limb of the diagonal band nucleus (MS/DBv) and theta discharges of GABAergic interneurons, and can be induced with cholinergic receptor agonists, it is not clear how the increased excitation of pyramidal cells could occur with increased discharges of GABAergic interneurons during theta waves. Here, we show that the characteristic theta activity in adult rat hippocampal CA1 pyramidal cells is associated with GABAergic postsynaptic depolarization and a shift of the reversal potential from Cl(-) toward HCO(3)(-) (whose ionic gradient is regulated by carbonic anhydrase). The theta activity was abolished by GABA(A) receptor antagonists and carbonic anhydrase inhibitors, but largely unaffected by blocking glutamate receptors. Carbonic anhydrase inhibition also impaired spatial learning in a water maze without affecting other sensory/locomotor behaviors. Thus HCO(3)(-)-mediated signaling, as regulated by carbonic anhydrase, through reversed polarity of GABAergic postsynaptic responses is implicated in both theta and memory consolidation in rat spatial maze learning. We suggest that this mechanism may be important for the phase forward shift of the place cell discharges for each theta cycle during the animal's traversal of the place field for that cell.

Acetazolamide↗
PubMed1992

Dissociation of spatial navigation and visual guidance performance in Purkinje cell degeneration (pcd) mutant mice.

Spatial learning in rodents requires normal functioning of hippocampal and cortical structures. Recent data suggest that the cerebellum may also be essential. Neurological mutant mice with dysgenesis of the cerebellum provide useful models to examine the effects of abnormal cerebellar function. Mice with one such mutation, Purkinje cell degeneration (pcd), in which Purkinje cells degenerate between the third and fourth postnatal weeks, were evaluated for performance of spatial navigation learning and visual guidance learning in the Morris maze swim-escape task. Unaffected littermates and C57BL/6J mice served as controls. Separate groups of pcd and control mice were tested at 30, 50 and 110 days of age. At all ages, pcd mice had severe deficits in distal-cue (spatial) navigation, failing to decrease path lengths over training and failing to express appropriate spatial biases on probe trials. On the proximal-cue (visual guidance) task, whenever performance differences between groups did occur, they were limited to the initial trials. The ability of the pcd mice to perform the proximal-cue but not the distal-cue task indicates that the massive spatial navigation deficit was not due simply to motor dysfunction. Histological evaluations confirmed that the pcd mutation resulted in Purkinje cell loss without significant depletion of cells in the hippocampal formation. These data provide further evidence that the cerebellum is vital for the expression of behavior directed by spatial cognitive processes.

Age Factors↗
PubMed1996

Maze procedures: the radial-arm and water maze compared.

Open mazes are primarily designed to measure place learning and memory, using environmental visuospatial cues. However, maze tasks differ along many dimensions, including (1) types of apparatus, which vary from arenas (water maze: WM) to highly structured routes (radial-arm maze: RAM); (2) availability of visuospatial, associative or sensory cues; (3) task requirements which range from spontaneous exploration to complex sequences of choices; and (4) motivation which may involve aversive escape, the opportunity to shelter or to discover novel objects or food at particular locations. Given this diversity, it is likely that mazes tap a variety of processes that contribute to, or affect spatial learning. Hence 'spatial' abilities measured in one procedure may not resemble those engaged in another, posing problems for the interpretation of drug- or lesion-induced deficits. This review compares two types of maze that exemplify key differences in procedure: the RAM and the WM. (1) Visuospatial, associative and sensory factors contributing to place learning in the two mazes are discussed, together with the types of search strategy that they foster, their differing motivation and vulnerability to effects of non-spatial factors, such as stress and training regime. (2) The equivalence of memory processes (acquisition, working and reference memory) assessed in different mazes is considered, and the extent that these may generalize to non-spatial tasks. (3) Differences in application of the two mazes are evaluated. The WM is well-adapted to the study of selective visuospatial factors in place learning and working memory, but less suitable for repeated measures or for assessment of long-term memory deficits. The RAM detects steady-state reference and working-memory deficits, and is suitable for repeated measures, at the expense of precise analysis of the nature of the processes involved.

Animals↗
PubMed2006

Impairments in water maze learning of aged rats that received dextromethorphan repeatedly during adolescent period.

RATIONALE: Dextromethorphan (DM), an over-the-counter cough suppressant, has been recently used as a drug of abuse by teenage groups in some countries, such as the United States, Canada, and Korea. We previously showed that repeated administration of DM, a noncompetitive antagonist of N-methyl-D-aspartate (NMDA) receptors, impairs spatial learning performance in adolescent rats. OBJECTIVES: In the present study, long-term adverse effects of repetitive DM use at adolescence were examined in rats. METHODS: Male and female Sprague-Dawley rat pups received either intraperitoneal DM (40 mg/kg) or saline daily during postnatal days 28-37, and were then subjected to the Morris water maze task at the age of 18 months. Expression levels of NMDAR1, functional subunit of NMDA receptors, in the prefrontal cortex and the hippocampus were examined by Western blot analysis. Changes in plasma corticosterone levels responding to stress were determined by radioimmunoassay. RESULTS: DM-experienced male rats exhibited deficits in the probe trial, and female rats in the initial learning and the reversal training, in water maze performance. Expression levels of NMDAR1 in the brain regions were significantly increased in DM-experienced rats, compared to control rats. Stress-induced increases in plasma corticosterone levels were blunted both in male and female DM rats. CONCLUSIONS: The results suggest that repeated administration of DM at high doses during adolescent period may induce permanent deficits in cognitive function and that increased expression of NMDAR1 in the prefrontal cortex and the hippocampus may take a role in DM-induced memory deficits.

Animals↗
PubMed1997

Mildly impaired water maze performance in male Fmr1 knockout mice.

Fmr1 knockout mice constitute a putative model of fragile X syndrome, the most common form of heritable mental disability in humans. We have compared the performance of transgenic mice with an Fmr1 knockout with that of normal littermates in hidden- and visible-platform water maze learning, and showed that knockouts exhibit subnormal spatial learning abilities and marginal motor performance deficits. During 12 training trials of the hidden-platform task, escape latency and path length decreased significantly in knockouts and control littermates, and no effect of genotype was found. During four ensuing reversal trials, however, significant differences were found between knockouts and control littermates both in escape latency and path length. During the visible-platform condition, the reversal trials also revealed a difference between knockouts and normal littermates in escape latency, but not in path length. Possibly due to marginal motor incapacity, knockouts swam significantly slower than controls during these latter trials. During both probe trials of the hidden-platform task, knockouts as well as normal littermates spent more time in the target quadrant than in the other quadrants, and percent of time spent in the target quadrant was the same in both groups; swimming velocity was not significantly different between knockouts and normal littermates during these trials. Entries in the target area during the probe trials did show a significant effect of genotype on number of entries. The present results largely confirm and extend our previous findings. Impaired spatial abilities in Fmr1 knockouts might have been due to relatively low response flexibility or high memory interference in Fmr1 knockouts. It remains unclear, however, which brain region or neurochemical system might be involved in these disabilities. We conclude that Fmr1 knockout mice might be a valid model of fragile X mental retardation.

Animals↗
PubMed2003

Spatial pre-training attenuates hippocampal impairments in rats exposed to intermittent hypoxia.

Intermittent hypoxia (IH), such as occurs in sleep apnea, is associated with increased apoptosis and neurobehavioral impairments in rats. To determine whether pre-training (P) modifies the effect of IH on spatial learning, adult male rats were trained in a spatial version of the water maze, exposed to IH or room air (RA) for 14 days, and then trained in a novel spatial task. P-RA had lower initial pathlengths than naive RA (N-RA), which were similar in P-IH and N-IH, indicating an adverse effect of IH on retention of behavioral strategies to solve the maze. However, P-IH acquired the later spatial task faster than N-IH. Pre-training was associated with increased phosphorylation of the cAMP-response element binding protein (CREB) in the hippocampus. Further, IH-induced decreases in CREB phosphorylation were attenuated by pre-training. We conclude that prior exposure to the water maze behavioral requirements attenuates the behavioral deficits occurring after IH exposure.

Animals↗
PubMed2002

Learning power of single behavioral units in acquisition of a complex spatial behavior: an observational learning study in cerebellar-lesioned rats.

By combining an observational spatial learning paradigm with a cerebellar lesion that blocks the acquisition of new spatial strategies, it is possible to separate a complex spatial behavior into its fundamental units to study which relationships among units have to be maintained so that the entire behavior might be acquired. Normal rats were first allowed to observe demonstrator rats performing single explorative behaviors (circling, extended searching, direct finding), then were hemicerebellectomized and, finally, tested in the Morris water maze. In spite of the cerebellar lesion, the observer rats displayed exploration abilities that closely matched the previously observed behaviors. These results indicate that the single facets that form the strategy repertoire can be independently acquired.

Animals↗