Inactivation of the nucleus reuniens/rhomboid causes a delay-dependent impairment of spatial working memory

Layfield, Dylan; Patel, Monica; Hallock, Henry L.; Griffin, Amy L.

doi:10.1016/j.nlm.2015.09.007

Cited by 57 publications

(63 citation statements)

References 47 publications

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“…A growing number of behavioural studies has provided evidence that RE is indeed involved in cognitive functions, most likely by coordinating neuronal activities in hippocampus and mPFC (Dolleman-van der Weel et al, 2009;Davoodi et al 2011;Eleore et al 2011;Hembrook et al 2011;Loureiro et al 2012;Prasad et al 2012;Cholvin et al 2013;Hallock et al 2013;Xu and Sűdhof 2013;Saalmann 2014;Bobal and Savage 2015;Ito et al 2015;Layfield et al 2015;Prasad et al 2016). Because mPFC lacks a direct return projection to the hippocampus (Sesack et al 1989;Jay and Witter 1991), RE might relay mPFC-processed information back to the hippocampus as part of a closed CA1-mPFC-RE-CA1 circuit Xu and Sűdhof 2013).…”

Section: Functional Relevancementioning

confidence: 99%

“…Recent studies have indicated the importance of RE for cognitive processes, such as behavioural flexibility, strategy shifting, inhibitory response control, associative learning, memory consolidation, working memory, fear memory, memory generalization, goal-directed navigation, and executive behaviours (Dollemanvan der Weel et al 2009;Davoodi et al 2011;Eleore et al 2011;Hembrook et al 2011;Kincheski et al 2012;Loureiro et al 2012;Cholvin et al 2013;Hallock et al 2013;Prasad et al 2013;Varela et al 2013;Wheeler et al 2013;Xu and Sűdhof 2013;Duan et al 2015;Griffin 2015;Ito et al 2015;Layfield et al 2015;Anderson et al 2015;Prasad et al 2016). This variety of memory-related behaviours has also been associated with the interplay between the medial prefrontal cortex (mPFC) and the hippocampus (Jin and Maren 2015).…”

Section: Introductionmentioning

confidence: 99%

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Interaction of nucleus reuniens and entorhinal cortex projections in hippocampal field CA1 of the rat

Weel

Silva

2016

Brain Struct Funct

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The nucleus reuniens (RE) and entorhinal cortex (EC) provide monosynaptic excitatory inputs to the apical dendrites of pyramidal cells and to interneurons with dendrites in stratum lacunosum-moleculare (LM) of hippocampal field CA1. However, whether the RE and EC inputs interact at the cellular level is unknown. In this electrophysiological in vivo study, low frequency stimulation was used to selectively activate each projection at its origin; field excitatory postsynaptic potentials (fEPSPs) were recorded in CA1. We applied 1) paired pulses to RE or EC, 2) combined paired pulses to RE and EC, and 3) simultaneously paired pulses to RE/EC. The main findings are that: i) stimulation of either RE or EC evoked subthreshold fEPSPs, displaying paired pulse facilitation (PPF), ii) subthreshold fEPSPs evoked by combined stimulation did not display heterosynaptic PPF, and iii) simultaneous stimulation of RE/EC resulted in enhanced subthreshold fEPSPs in proximal LM displaying a nonlinear interaction.CSD analyses of RE/EC-evoked depth profiles revealed a nonlinear enlargement of the 'LM sink-radiatum source' configuration and the appearance of an additional small sink-source pair close to stratum pyramidale, likely reflecting (peri)somatic inhibition. The nonlinear interaction between both inputs indicates that RE and EC axons form synapses, at least partly, onto the same dendritic compartments of CA1 pyramidal cells. We propose that low frequency activation of the RE-CA1 input facilitates the entorhinal-hippocampal dialogue, and may synchronize the neocortical-hippocampal slow oscillation which is relevant for hippocampal-dependent memory consolidation.

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Section: Functional Relevancementioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Interaction of nucleus reuniens and entorhinal cortex projections in hippocampal field CA1 of the rat

Weel

Silva

2016

Brain Struct Funct

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“…Inactivation of RE/RH, the hippocampus or the mPFC impaired the shift to a place response, indicating that disruption of the HF, the mPFC, or the RE-mediated communication between them altered performance on this spatial WM task. Finally, Layfield et al (2015) recently reported that suppression of RE/RH did not disrupt performance on continuous version of a T-maze alternation task, which appears to depend on the mPFC, but significantly altered performance on the delayed version of the task which reportedly enlists both the HF and the mPFC (Aggelton et al, 1986; Brito and Brito, 1990; Sanchez-Santad et al, 1997; Hock and Bunsey, 1998; Lee and Kesner, 2003; Yoon et al, 2008). …”

Section: Introductionmentioning

confidence: 96%

“…Based on these patterns of connections, several recent behavioral studies have examined the role of RE (and the dorsally adjacent rhomboid nucleus, RH) in various spatial working memory tasks (Hembrook and Mair, 2011; Hembrook et al, 2012; Loureiro et al, 2012; Cholvin et al, 2013; Hallock et al, 2013; Layfield et al, 2015). The general conclusion from these studies is that RE/RH is most directly involved in those tasks that involve the cooperative actions of the mPFC and the hippocampus (for review, Cassel et al, 2013; Vertes et al 2015; Griffin, 2015).…”

Section: Introductionmentioning

confidence: 99%

Lesions of the ventral midline thalamus produce deficits in reversal learning and attention on an odor texture set shifting task

2016

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The nucleus reuniens (RE) of the ventral midline thalamus in strongly reciprocally connected with the hippocampus (HF) and the medial prefrontal cortex (mPFC) and has been shown to mediate the transfer of information between these structures. It has become increasingly well established that RE serves a critical role in mnemonic tasks requiring the interaction of the HF and mPFC, but not tasks relying solely on the HF. Very few studies have addressed the independent actions of RE on prefrontal executive functioning. The present report examined the effects of lesions of the ventral midline thalamus, including RE and the dorsally adjacent rhomboid nucleus (RH) in rats on attention and behavioral flexibility using the attentional set shifting task (AST). The task uses odor and tactile stimuli to test for attentional set formation, attentional set shifting, behavioral flexibility and reversal learning. By comparison with sham controls, lesioned rats were significantly impaired on reversal learning and intradimensional (ID) set shifting. Specifically, RE/RH lesioned rats were impaired on the first reversal stage of the task which required a change in response strategy to select a previously non-rewarded stimulus for reward. RE/RH lesioned rats also exhibited deficits in the ability to transfer or generalize rules of the task which consists of making the same modality-based choices (e.g., odor vs. tactile) to different sets of stimuli in the ID stage of the task. These results demonstrate that in addition to its role in tasks dependent on HF-mPFC interactions, RE/RH is also critically involved cognitive/executive functions associated with the medial prefrontal cortex. As such, the deficits in the AST task produced by RE/RH lesions suggest the ventral midline thalamus directly contributes to flexible goal directed behavior.

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“…We compared experimental and control rats on operant behavioral tasks assessing visual attention and working memory, associative learning and decision-making. We also tested rats on a radial arm maze as several studies indicate a role for the NRe in spatial memory (Hembrook and Mair, 2011; Loureiro et al, 2012; Layfield et al, 2015; Ito et al, 2015). We report several features that distinguish NRe lesions from those of its projection targets.…”

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confidence: 99%

Midline thalamic reuniens lesions improve executive behaviors

2017

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The role of the thalamus in complex cognitive behavior is a topic of increasing interest. Here we demonstrate that lesions of the nucleus reuniens (NRe), a midline thalamic nucleus interconnected with both hippocampal and prefrontal circuitry, lead to enhancement of executive behaviors typically associated with the prefrontal cortex. Rats were tested on four behavioral tasks: (1) the combined attention-memory (CAM) task, which simultaneously assessed attention to a visual target and memory for that target over a variable delay; (2) spatial memory using a radial arm maze, (3) discrimination and reversal learning using a touchscreen operant platform, and (4) decision-making with delayed outcomes. Following NRe lesions, the animals became more efficient in their performance, responding with shorter reaction times but also less impulsively than controls. This change, combined with a decrease in perseverative responses, led to focused attention in the CAM task and accelerated learning in the visual discrimination task. There were no observed changes in tasks involving either spatial memory or value-based decision making. These data complement ongoing efforts to understand the role of midline thalamic structures in human cognition, including the development of thalamic stimulation as a therapeutic strategy for acquired cognitive disabilities (Schiff, 2008; Mair et al., 2011), and point to the NRe as a potential target for clinical intervention.

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Inactivation of the nucleus reuniens/rhomboid causes a delay-dependent impairment of spatial working memory

Cited by 57 publications

References 47 publications

Interaction of nucleus reuniens and entorhinal cortex projections in hippocampal field CA1 of the rat

Interaction of nucleus reuniens and entorhinal cortex projections in hippocampal field CA1 of the rat

Lesions of the ventral midline thalamus produce deficits in reversal learning and attention on an odor texture set shifting task

Midline thalamic reuniens lesions improve executive behaviors

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