Lesions of the dorsomedial striatum delay spatial learning and render cue-based navigation inflexible in a water maze task in mice (original) (raw)
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Homologous involvement of striatum and prefrontal cortex in rodent and human water maze learning
Proceedings of the National Academy of Sciences, 2013
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.
PloS one, 2017
Neurons in anterior cingulate cortex (aCC) project to dorsomedial striatum (DMS) as part of a corticostriatal circuit with putative roles in learning and other cognitive functions. In the present study, the spatial-cognitive importance of aCC and DMS was assessed in the hidden-platform version of the Morris water maze (MWM). Brain lesion experiments that focused on areas of connectivity between these regions indicated their involvement in spatial cognition. MWM learning curves were markedly delayed in DMS-lesioned mice in the absence of other major functional impairments, whereas there was a more subtle, but still significant influence of aCC lesions. Lesioned mice displayed impaired abilities to use spatial search strategies, increased thigmotaxic swimming, and decreased searching in the proximity of the escape platform. Additionally, aCC and DMS activity was compared in mice between the early acquisition phase (2 and 3 days of training) and the over-trained high-proficiency phase ...
Dissociation of Hippocampal and Striatal Contributions to Spatial Navigation in the Water Maze
Neurobiology of Learning and Memory, 1996
where the platform was formerly positioned. The results suggest that the hippocampus mediates the allocentric Two experiments were conducted to compare the effects of fornix/fimbria and caudate-putamen lesions in Long -spatial component of the water maze place task while the dorsomedial striatum may play an important role in the Evans hooded rats (Rattus norvegicus) trained on two water maze tasks that differed in the type of spatial local-acquisition of the procedural aspects of both place and cue versions of the task. ᭧ 1996 Academic Press, Inc. ization required for optimum solution. In Experiment 1, the lesioned rats and surgical controls were trained on the standard place task in the water maze (Morris, 1981) and given two postacquisition tests (a platform removal It has been suggested that both the hippocampus probe and platform relocation test). In Experiment 2, rats and dorsal striatum (caudate-putamen) of the rat with similar lesions and control rats were trained on a make important contributions to spatially organized modified cue navigation task. Fornix/fimbria lesions imbehavior, albeit in different ways. The hippocampus paired a late stage of place task acquisition but did not has been hypothesized to be the neural substrate for impair acquisition of the cue task. Caudate-putamen lesions resulted in a severe place acquisition impairment allocentric spatial localization (i.e., cognitive mapand a transient cue acquisition impairment, both of ping; O' Keefe & Nadel, 1978), whereas the caudate which were characterized by an initial tendency to swim nucleus has been hypothesized to play a critical role near the wall of the pool. Post-hoc analyses of the direcin egocentric spatial orientation (Kesner & DiMattion and angles of departure from the start points sug- tia, 1987; Potegal, , 1982. gested that rats with fornix/fimbria lesions used non-allo-O' Keefe and Nadel's (1978) theory is supported by centric spatial strategies to solve the place task. These the finding that damage to the hippocampal system rats also demonstrated a significantly weakened spatial results in impairments on tasks that require the use bias for the former training quadrant on the platform of the relations between ambient distal stimuli to removal probe and reduced flexibility in navigating to a locate a particular goal in space. One such task is novel platform location on the platform relocation test.
Behavior strategy learning in rat: effects of lesions of the dorsal striatum or dorsal hippocampus
Behavioural Processes, 2004
Depending on task demands, there is a growing body of evidence suggesting that the dorsal striatum plays a critical role in not only learning new response strategies but also in the inhibition of pre-existing strategies when a shift in strategy is required. The present experiment examined the effects of lesions of the dorsal striatum or dorsal hippocampus on acquisition of a response-learning rule and a place-learning rule in a Greek Cross version of the Morris water maze. Specifically, adult Long-Evans rats were prepared with either sham lesions or lesions to one of two subcortical areas of the brain considered necessary for processing nondeclarative or declarative memories, the dorsal striatum or the hippocampus, respectively. An analysis of the trial 2 performance pooled across reversals revealed hippocampus lesions induced accelerated acquisition when a response-learning rule was required. A much smaller enhancement effect was observed in dorsal striatum-lesioned animals in the place-learning paradigm. Dorsal hippocampus-and dorsal striatum-lesioned animals were highly impaired on place learning and response learning, respectively. The present results are congruent with a growing body of literature suggesting that different anatomical substrates are involved in the acquisition and maintenance of different types of information, that these processes can occur simultaneously and in parallel, and that the dorsal striatum is necessary for the mediation of stimulus-response learning, while the hippocampus is necessary to mediate the expression of place learning.
2015
Both egocentric route-based learning and spatial learning, as assessed by the Cincinnati water maze (CWM) and Morris water maze (MWM), respectively, are impaired following an 80% dopamine (DA) loss in the neostriatum after 6-hydroxydopamine (6-OHDA) administration in rats. The dorsolateral striatum (DLS) and the dorsomedial striatum (DMS) are implicated in different navigational learning types, namely the DLS is implicated in egocentric learning while the DMS is implicated in spatial learning. This experiment tested whether selective DA loss through 6-OHDA lesions in the DMS or DLS would impair one or both types of navigation. Both DLS and DMS DA loss significantly impaired route-based CWM learning, without affecting spatial or cued MWM performance. DLS 6-OHDA lesions produced a 75% DA loss in this region, with no changes in other monoamine levels in the DLS or DMS. DMS 6-OHDA lesions produced a 62% DA loss in this region, without affecting other monoamine levels in the DMS or DLS. The results indicate a role for DA in DLS and DMS regions in route-based egocentric but not spatial learning and memory. Spatial learning deficits may require more pervasive monoamine reductions within each region before deficits are exhibited. This is the first study to implicate DLS and DMS DA in route-based egocentric navigation.
Frontiers in Behavioral Neuroscience
The participation of the prefrontal cortex (PFC), hippocampus, and dorsal striatum in switching the learning task from cued to place learning were examined in C57BL/6 and DBA/2 mice, by assessing changed levels of phosphorylated CREB (pCREB). Mice of both strains first received cued training in a water maze for 4 days (4 trials per day), and were then assigned to one of four groups, one with no place training, and three with different durations of place training (2, 4, or 8 days). Both strains showed equal performance in cued training. After the switch to place training, C57BL/6 mice with 2 or 4 days of training performed significantly better than DBA/2 mice, but their superiority disappeared during the second half of an 8 days-place training period. The pCREB levels of these mice were measured 30 min after place training and compared with those of mice that received only cued training. Changes in pCREB levels of C57BL/6 mice were greater in the hippocampal CA3, hippocampal dentate gyrus, orbitofrontal and medial PFC than those of DBA/2 mice, when mice of both received the switched place training for 2 days. We further investigated the roles of orbitofrontal and medial PFC among these brain regions showing strain differences, by destroying each region using selective neurotoxins. C57BL/6 mice with orbitofrontal lesions were slower to acquire the place learning and continued to use the cued search acquired during the cued training phase. These findings indicate that mouse orbitofrontal cortex (OFC) pCREB is associated with behavioral flexibility such as the ability to switch a learning task.
Multimodal Plasticity in Dorsal Striatum While Learning a Lateralized Navigation Task
The Journal of neuroscience : the official journal of the Society for Neuroscience, 2015
Growing evidence supports a critical role for the dorsal striatum in cognitive as well as motor control. Both lesions and in vivo recordings demonstrate a transition in the engaged dorsal striatal subregion, from dorsomedial to dorsolateral, as skill performance shifts from an attentive phase to a more automatic or habitual phase. What are the neural mechanisms supporting the cognitive and behavioral transitions in skill learning? To pursue this question, we used T-maze training during which rats transition from early, attentive (dorsomedial) to late habitual (dorsolateral) performance. Following early or late training, we performed the first direct comparison of bidirectional synaptic plasticity in striatal brain slices, and the first evaluation of striatal synaptic plasticity by hemisphere relative to a learned turn. Consequently, we find that long-term potentiation and long-term depression are independently modulated with learning rather than reciprocally linked as previously sug...
Selective lesions of the dorsomedial striatum impair serial spatial reversal learning in rats
Behavioural brain research, 2010
Impairments in reversal learning have been attributed to orbitofrontal cortex (OFC) dysfunction in many species. However, the role of subcortical areas interconnected with the OFC such as the striatum remains poorly understood. This study directly evaluated the contribution of core and shell sub-regions of the nucleus accumbens (NAc), dorsomedial (DMS) and dorsolateral (DLS) striatum to reversal learning of an instrumental two-lever spatial discrimination task in rats. Selective NAc core, DMS and DLS lesions were achieved with microinjections of quinolinic acid and NAc shell lesions with ibotenic acid. Damage to NAc core or shell did not affect retention of a previously acquired instrumental spatial discrimination. In contrast, DLS and DMS lesions produced changes in aspects of discrimination performance such as the latency to collect earned food pellets. Neither NAc core or shell lesions nor DLS lesions affected the main indices of reversal performance. Conversely, DMS lesion rats ...