Cooperation between the Hippocampus and the Striatum during Episodic Encoding

Sadeh, Talya; Shohamy, Daphna; Levy, Dana Rubi; Reggev, Niv; Maril, Anat

doi:10.1162/jocn.2010.21549

Cited by 91 publications

(65 citation statements)

References 76 publications

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“…Interpreting our findings based on the model of competition between these regions (Lee et al, 2008;Poldrack et al, 2001) suggests that in CD, increased potential to use striatum-based strategies for learning may inhibit activity within MTL, although an independent dysfunction of MTL cannot be excluded. Conversely, interpreting our findings based on a model of cooperation between these brain regions (Sadeh et al, 2011;Voermans et al, 2004) would suggest that in CD, inefficient representations of MTL-based strategies for learning may produce a compensatory modulation of striatal activity in the service of maintaining normal behavioral performance on the task, particularly when the task is difficult (as it was in our control condition). Cortical activations also differed across groups.…”

Section: Searching the Maze For Navigational Cuesmentioning

confidence: 72%

Neural Correlates of Reward-Based Spatial Learning in Persons with Cocaine Dependence

Tau

Marsh

Wang

et al. 2013

Neuropsychopharmacol

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Dysfunctional learning systems are thought to be central to the pathogenesis of and impair recovery from addictions. The functioning of the brain circuits for episodic memory or learning that support goal-directed behavior has not been studied previously in persons with cocaine dependence (CD). Thirteen abstinent CD and 13 healthy participants underwent MRI scanning while performing a task that requires the use of spatial cues to navigate a virtual-reality environment and find monetary rewards, allowing the functional assessment of the brain systems for spatial learning, a form of episodic memory. Whereas both groups performed similarly on the reward-based spatial learning task, we identified disturbances in brain regions involved in learning and reward in CD participants. In particular, CD was associated with impaired functioning of medial temporal lobe (MTL), a brain region that is crucial for spatial learning (and episodic memory) with concomitant recruitment of striatum (which normally participates in stimulus-response, or habit, learning), and prefrontal cortex. CD was also associated with enhanced sensitivity of the ventral striatum to unexpected rewards but not to expected rewards earned during spatial learning. We provide evidence that spatial learning in CD is characterized by disturbances in functioning of an MTL-based system for episodic memory and a striatum-based system for stimulus-response learning and reward. We have found additional abnormalities in distributed cortical regions. Consistent with findings from animal studies, we provide the first evidence in humans describing the disruptive effects of cocaine on the coordinated functioning of multiple neural systems for learning and memory.

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Section: Searching the Maze For Navigational Cuesmentioning

confidence: 72%

Neural Correlates of Reward-Based Spatial Learning in Persons with Cocaine Dependence

Tau

Marsh

Wang

et al. 2013

Neuropsychopharmacol

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“…Previous studies showed that several striatal subregions (especially caudate) and the hippocampus interact during episodic memory (41)(42)(43)(44)(45)(46), and considerable overlap has been observed in the pattern of functional connectivity for hippocampal and caudate seeds (47). This suggests that these regions are part of a shared functional network.…”

Section: Discussionmentioning

confidence: 94%

Dopamine D2 receptor availability is linked to hippocampal–caudate functional connectivity and episodic memory

Nyberg

Karalija

Salami

et al. 2016

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

144

131

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D1 and D2 dopamine receptors (D1DRs and D2DRs) may contribute differently to various aspects of memory and cognition. The D1DR system has been linked to functions supported by the prefrontal cortex. By contrast, the role of the D2DR system is less clear, although it has been hypothesized that D2DRs make a specific contribution to hippocampus-based cognitive functions. Here we present results from 181 healthy adults between 64 and 68 y of age who underwent comprehensive assessment of episodic memory, working memory, and processing speed, along with MRI and D2DR assessment with [ 11 C]raclopride and PET. Caudate D2DR availability was positively associated with episodic memory but not with working memory or speed. Whole-brain analyses further revealed a relation between hippocampal D2DR availability and episodic memory. Hippocampal and caudate D2DR availability were interrelated, and functional MRIbased resting-state functional connectivity between the ventral caudate and medial temporal cortex increased as a function of caudate D2DR availability. Collectively, these findings indicate that D2DRs make a specific contribution to hippocampus-based cognition by influencing striatal and hippocampal regions, and their interactions.dopamine | memory | hippocampus D opamine (DA) plays a key role in several cognitive processes (1-4). Reductions of D1 and D2 DA receptors (D1DRs and D2DRs) in aging (5-7) have been linked to agerelated cognitive deficits (8, 9). The D1DR system has been related to functions supported by the prefrontal cortex (PFC), such as working memory and executive functions (10-12), which may reflect the relatively high density of D1DRs in the PFC (13). However, the role of D2DRs is far less clear. D2DRs are present in the PFC at very low densities (13), and evidence supporting a role for the D2DR system in working memory and executive functions is elusive (10). Pharmacological (14, 15) and PET studies assessing striatal D2DR availability (or binding potential to nondisplacable tissue uptake; BP ND ) with [ 11 C]raclopride (16, 17) have yielded mixed findings in relation to cognition. It has been hypothesized that D2DRs make a specific contribution to hippocampus-based cognitive functions (10,18,19). Supporting these claims, positive links between D2DR BP ND and episodic memory are commonly observed (20-23). PET imaging of hippocampal D2DR BP ND also provides support for this hypothesis, although some studies indicate that hippocampal D2DRs may be related to both episodic memory and PFC-based executive functions (22, 23), including verbal working memory (24). Medial temporal lobe regions have been implicated in working memory (25,26), and D2DR-mediated modulation may be exerted via hippocampal-cortical pathways (27). In addition, a [ 11 C]raclopride task-activation PET study demonstrated contributions of striatal D2DRs to a verbal working-memory task (11).Taken together, the specific role of the D2DR system in cognition remains unclear, likely due to the fact that past studies included small and age-hetero...

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“…Two recent studies found increased correlation between the activity of the dopaminergic system and the hippocampus during successful encoding that required integration of information. The first study (Shohamy and Wagner, 2008) showed an increased correlation between activity in the hippocampus and the dopaminergic midbrain during successful versus unsuccessful generalization of associations, and the second study (Sadeh et al, 2011) found an increased correlation between the putamen and the hippocampus during successful episodic encoding. Although these studies did not report such correlations in the caudate nucleus, as part of the dopaminergic system, it is strongly connected to both the dopaminergic midbrain and the putamen.…”

Section: Discussionmentioning

confidence: 99%

Constructing Realistic Engrams: Poststimulus Activity of Hippocampus and Dorsal Striatum Predicts Subsequent Episodic Memory

Ben-Yakov

Dudai²

2011

Journal of Neuroscience

204

202

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Encoding of real-life episodic memory commonly involves integration of information as the episode unfolds. Offline processing immediately following event offset is expected to play a role in encoding the episode into memory. In this study, we examined whether distinct human brain activity time-locked to the offset of short narrative audiovisual episodes could predict subsequent memory for the gist of the episodes. We found that a set of brain regions, most prominently the bilateral hippocampus and the bilateral caudate nucleus, exhibit memory-predictive activity time-locked to the stimulus offset. We propose that offline activity in these regions reflects registration to memory of integrated episodes.

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Cooperation between the Hippocampus and the Striatum during Episodic Encoding

Cited by 91 publications

References 76 publications

Neural Correlates of Reward-Based Spatial Learning in Persons with Cocaine Dependence

Neural Correlates of Reward-Based Spatial Learning in Persons with Cocaine Dependence

Dopamine D2 receptor availability is linked to hippocampal–caudate functional connectivity and episodic memory

Constructing Realistic Engrams: Poststimulus Activity of Hippocampus and Dorsal Striatum Predicts Subsequent Episodic Memory

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