Both the dorsal hippocampus and the dorsolateral striatum are needed for rat navigation in the Morris water maze

Miyoshi, Edmar; Wietzikoski, Evellyn Claudia; Bortolanza, Mariza; Boschen, Suelen Lúcio; Canteras, Newton S.; Izquierdo, Iván; Cunha, Cláudio Da

doi:10.1016/j.bbr.2011.09.011

Cited by 57 publications

(39 citation statements)

References 38 publications

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“…Contrary to this view, we found that dorsomedial but not dorsolateral striatum makes a critical contribution to the early phase of place learning (SI Discussion). This result is consistent with previous reports of impaired expression of place learning after dorsomedial striatum lesions (18)(19)(20)(35)(36)(37). For example, when rats performed a water maze task designed to test for a preference between previously learned response-based and place-based strategies, dorsomedial striatum lesions resulted in a lower likelihood of choosing a place-based strategy (4,19).…”

Section: Discussionsupporting

confidence: 91%

Homologous involvement of striatum and prefrontal cortex in rodent and human water maze learning

Woolley¹,

Laeremans²,

Gantois

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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The multiple memory systems hypothesis posits that dorsal striatum and hippocampus are central nodes in independent memory systems, supporting response-based and place-based learning, respectively. Although our understanding of the function of hippocampus within this framework is relatively well established, the contribution of dorsal striatum is less clear. This in part seems to be due to the heterogeneous nature of dorsal striatum, which receives extensive topographically organized projections from higher cortical areas. Here we quantified neural activity in the intact brain while mice and humans acquired analogous versions of the Morris water maze. We found that dorsomedial striatum and medial prefrontal cortex support the initial acquisition of what is typically considered a hippocampus-dependent spatial learning task. We suggest that the circuit involving dorsomedial striatum and medial prefrontal cortex identified here plays a more task-independent role in early learning than currently thought. Furthermore, our results demonstrate that dorsomedial and dorsolateral striatum serve fundamentally different roles during place learning. The remarkably high degree of anatomical overlap in brain function between mouse and human observed in our study emphasizes the extent of convergence achievable with a well-matched multilevel approach.functional MRI | immediate early gene | navigation T he multiple memory systems hypothesis posits that hippocampus and dorsal striatum are central nodes in independent memory systems, each supporting different aspects of learning and memory formation (1-4). In the context of spatial learning, the hippocampus supports place-based behavioral strategies relying on learning the general layout of the environment, whereas the dorsal striatum supports response-based behavioral strategies driven by task-specific stimuli (5-12). Although the dorsal striatum is often referred to as a unitary structure within the multiple memory systems framework, there is considerable evidence in rodents and humans that it is composed of functional subdivisions that support different aspects of learning (13-20).Here we conducted parallel experiments in mouse and human to test whether dorsomedial and dorsolateral striatum make distinct contributions during early (initial acquisition) and late (overtraining) phases of place learning in the intact brain. Subjects performed the classic hippocampus-dependent hidden platform version of the Morris water maze, which was matched between species with respect to behavioral processing demands (9). This widely used paradigm has served a critical role in the study of neurobiological aspects of learning and memory over the past 25 years (21,22).Although it is well established that hippocampus supports the spatial processing demands of the water maze, much less is known about the precise contribution of dorsomedial and dorsolateral striatum during the early and late phases of learning in the hiddenplatform version of the task. If dorsomedial striatum plays a general role in ...

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Section: Discussionsupporting

confidence: 91%

Homologous involvement of striatum and prefrontal cortex in rodent and human water maze learning

Woolley¹,

Laeremans²,

Gantois

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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“…In aged rats, we also found a negative correlation between the number of striatal ChAT-positive interneurons and water maze performance during the two training periods, as reported earlier (Colombo and Gallagher 1998;Stemmelin et al 2000). Even though the MWM task is generally considered to depend on hippocampal functions, other structures, among which the striatum, are known to contribute (e.g., Devan et al 1996;Shirakawa and Ichitani 2004;Miyoshi et al 2012). Thus, it can be suggested that the positive effect of enriched environment on water maze learning may also be related to the environmental impact on the survival of striatal cholinergic neurons.…”

Section: Spatial Cognition and Forebrain Cholinergic Neuronssupporting

confidence: 87%

Lifelong environmental enrichment in rats: impact on emotional behavior, spatial memory vividness, and cholinergic neurons over the lifespan

Harati

Barbelivien

Herbeaux

et al. 2012

AGE

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We assessed lifelong environmental enrichment effects on possible age-related modifications in emotional behaviors, spatial memory acquisition, retrieval of recent and remote spatial memory, and cholinergic forebrain systems. At the age of 1 month, Long-Evans female rats were placed in standard or enriched rearing conditions and tested after 3 (young), 12 (middle-aged), or 24 (aged)months. Environmental enrichment decreased the reactivity to stressful situations regardless of age. In the water maze test, it delayed the onset of learning deficits and prevented age-dependent spatial learning and recent memory retrieval alterations. Remote memory retrieval, which was altered independently of age under standard rearing conditions, was rescued by enrichment in young and middle-aged, but unfortunately not aged rats. A protected basal forebrain cholinergic system, which could well be one out of several neuronal manifestations of lifelong environmental enrichment, might have contributed to the behavioral benefits of this enrichment.

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“…The ability of the mice to perform in the Morris water maze test is thought to require competent hippocampal, striatal, and cortical functions, which are thought to be altered with age (Winocur and Moscovitch 1990;Lee et al 1994;Burke and Barnes 2006;Miyoshi et al 2012). The results indicated that a high dose of CoQ reversed age-related inefficiency in locating the hidden platform during the training phase.…”

Section: Discussionmentioning

confidence: 97%

Coenzyme Q10 supplementation reverses age-related impairments in spatial learning and lowers protein oxidation

Shetty

Forster

Sumien

2012

AGE

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Coenzyme Q10 (CoQ) is widely available as a dietary supplement and remains under consideration as a treatment for age-associated neurodegenerative conditions. However, no studies have determined if supplementation, initiated relatively late in life, could have beneficial effects on mild functional impairments associated with normal brain aging. Accordingly, the current study assessed the effect of CoQ intake in older mice for which cognitive and psychomotor impairments were already evident. Separate groups of young (3.5 months) and relatively old mice (17.5 months) were fed a control diet or a diet supplemented with low (0.72 mg/g) or high (2.81 mg/g) concentrations of CoQ for 15 weeks. After 6 weeks, the mice were given tests for spatial learning (Morris water maze), spontaneous locomotor activity, motor coordination, and startle reflex. Age-related impairments in cognitive and psychomotor functions were evident in the 17.5-month-old mice fed the control diet, and the low-CoQ diet failed to affect any aspect of the impaired performance. However, in the Morris water maze test, old mice on the high-CoQ diet swam to the safe platform with greater efficiency than the mice on the control diet. The old mice supplemented with the highCoQ diet did not show improvement when spatial performance was measured using probe trials and failed to show improvement in other tests of behavioral performance. Protein oxidative damage was decreased in the mitochondria from the heart, liver, and skeletal muscle of the high-CoQ-supplemented mice and, to some extent, in the brain mitochondria. Contrasting with the deleterious effect of long-term CoQ supplementation initiated during young adulthood previously published, this study suggests that CoQ improves spatial learning and attenuates oxidative damage when administered in relatively high doses and delayed until early senescence, after agerelated declines have occurred. Thus, in individuals with age-associated symptoms of cognitive decline, highCoQ intake may be beneficial.

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Both the dorsal hippocampus and the dorsolateral striatum are needed for rat navigation in the Morris water maze

Cited by 57 publications

References 38 publications

Homologous involvement of striatum and prefrontal cortex in rodent and human water maze learning

Homologous involvement of striatum and prefrontal cortex in rodent and human water maze learning

Lifelong environmental enrichment in rats: impact on emotional behavior, spatial memory vividness, and cholinergic neurons over the lifespan

Coenzyme Q10 supplementation reverses age-related impairments in spatial learning and lowers protein oxidation

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