Optogenetic perturbation of projections from thalamic nucleus reuniens to hippocampus disrupts spatial working memory retrieval more than encoding

Rahman, Faiyaz; Nanu, Roshan; Schneider, Nathan A.; Katz, Donald B.; Lisman, John; Pi, Hyun Jae

doi:10.1016/j.nlm.2021.107396

Cited by 9 publications

(7 citation statements)

References 28 publications

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“…Alternatively, studies have shown that increased delta power may also contribute to working memory performance. In fact, the stimulation of delta to the thalamic nucleus reuniens, an indirect ACC–hippocampal pathway, leads to elevated delta in the hippocampus and spatial working memory impairments 66 , 67 . Thus, this imbalance may be attributed to both higher delta power and lower theta power.…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, it is less clear how neuroinflammation might affect the ACC or interactions between the hippocampus and ACC, which are likely mediated by thalamic connections 55 . Intriguingly, abnormal delta activity from the thalamus into the hippocampus has been linked with impaired working memory retrieval 67 , perhaps hyperglycemia is affecting the thalamus leading to the increase in hippocampal delta power and altered hippocampal–ACC theta interactions. While more work is needed to better understand how neuroinflammation relates to network activity, there have been multiple reports revealing neuroinflammation-linked memory deficits in rodents 115 , 116 and in humans 117 .…”

Section: Discussionmentioning

confidence: 99%

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Altered theta rhythm and hippocampal-cortical interactions underlie working memory deficits in a hyperglycemia risk factor model of Alzheimer’s disease

et al. 2021

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Diabetes mellitus is a metabolic disease associated with dysregulated glucose and insulin levels and an increased risk of developing Alzheimer’s disease (AD) later in life. It is thought that chronic hyperglycemia leads to neuroinflammation and tau hyperphosphorylation in the hippocampus leading to cognitive decline, but effects on hippocampal network activity are unknown. A sustained hyperglycemic state was induced in otherwise healthy animals and subjects were then tested on a spatial delayed alternation task while recording from the hippocampus and anterior cingulate cortex (ACC). Hyperglycemic animals performed worse on long delay trials and had multiple electrophysiological differences throughout the task. We found increased delta power and decreased theta power in the hippocampus, which led to altered theta/delta ratios at the end of the delay period. Cross frequency coupling was significantly higher in multiple bands and delay period hippocampus-ACC theta coherence was elevated, revealing hypersynchrony. The highest coherence values appeared long delays on error trials for STZ animals, the opposite of what was observed in controls, where lower delay period coherence was associated with errors. Consistent with previous investigations, we found increases in phosphorylated tau in STZ animals’ hippocampus and cortex, which might account for the observed oscillatory and cognitive changes.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Altered theta rhythm and hippocampal-cortical interactions underlie working memory deficits in a hyperglycemia risk factor model of Alzheimer’s disease

et al. 2021

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“…Additionally, WM deficits are accompanied by poor interregional synchrony in rodent models of schizophrenia ( Sigurdsson et al, 2010 ). However, optogenetically inducing delta oscillations in the thalamic projection to the hippocampus impairs WM performance in rodents- so not all oscillatory manipulations are beneficial ( Duan et al, 2015 ; Rahman et al, 2021 ). In summary, a variety of brain disorders characterized by WM impairments also show evidence of changes in synchronization between brain areas, supporting the hypothesis that such synchronization is important for WM performance.…”

Section: Dysfunctions In Oscillations and Synchrony During Working Memory Occur In Brain Disordersmentioning

confidence: 99%

Dependence of Working Memory on Coordinated Activity Across Brain Areas

Rezayat

Clark

Dehaqani

et al. 2022

Front. Syst. Neurosci.

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Neural signatures of working memory (WM) have been reported in numerous brain areas, suggesting a distributed neural substrate for memory maintenance. In the current manuscript we provide an updated review of the literature focusing on intracranial neurophysiological recordings during WM in primates. Such signatures of WM include changes in firing rate or local oscillatory power within an area, along with measures of coordinated activity between areas based on synchronization between oscillations. In comparing the ability of various neural signatures in any brain area to predict behavioral performance, we observe that synchrony between areas is more frequently and robustly correlated with WM performance than any of the within-area neural signatures. We further review the evidence for alteration of inter-areal synchrony in brain disorders, consistent with an important role for such synchrony during behavior. Additionally, results of causal studies indicate that manipulating synchrony across areas is especially effective at influencing WM task performance. Each of these lines of research supports the critical role of inter-areal synchrony in WM. Finally, we propose a framework for interactions between prefrontal and sensory areas during WM, incorporating a range of experimental findings and offering an explanation for the observed link between intra-areal measures and WM performance.

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“…Specifically, Maisson et al ( 2018 ) using a delayed non-match to position (DNMP) T-maze task, showed that optogenetic inhibition of RE during the sample phase, but not during the delay or choice phases (retrieval) of the task, significantly impaired performance on the task, and concluded that RE mainly contributes to the encoding of spatial information in SWM tasks. Conversely, Rahman et al ( 2021 ) recently demonstrated that optogenetically stimulating RE hippocampal-projecting fibers at delta frequency (3–4 Hz) in mice, which had previously been shown to disrupt memory processing in rats (Duan et al, 2015 ), significantly impaired the retrieval but not the encoding of memory on a spatial Y-maze task. Lastly, Jayachandran et al ( 2019 ) described the involvement of RE in the temporal coding of working memory.…”

Section: The Ventral Midline Thalamus: Reuniens and Rhomboid Nucleimentioning

confidence: 99%

Structural and functional organization of the midline and intralaminar nuclei of the thalamus

Vertes

Linley

Rojas

2022

Front. Behav. Neurosci.

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The midline and intralaminar nuclei of the thalamus form a major part of the “limbic thalamus;” that is, thalamic structures anatomically and functionally linked with the limbic forebrain. The midline nuclei consist of the paraventricular (PV) and paratenial nuclei, dorsally and the rhomboid and nucleus reuniens (RE), ventrally. The rostral intralaminar nuclei (ILt) consist of the central medial (CM), paracentral (PC) and central lateral (CL) nuclei. We presently concentrate on RE, PV, CM and CL nuclei of the thalamus. The nucleus reuniens receives a diverse array of input from limbic-related sites, and predominantly projects to the hippocampus and to “limbic” cortices. The RE participates in various cognitive functions including spatial working memory, executive functions (attention, behavioral flexibility) and affect/fear behavior. The PV receives significant limbic-related afferents, particularly the hypothalamus, and mainly distributes to “affective” structures of the forebrain including the bed nucleus of stria terminalis, nucleus accumbens and the amygdala. Accordingly, PV serves a critical role in “motivated behaviors” such as arousal, feeding/consummatory behavior and drug addiction. The rostral ILt receives both limbic and sensorimotor-related input and distributes widely over limbic and motor regions of the frontal cortex—and throughout the dorsal striatum. The intralaminar thalamus is critical for maintaining consciousness and directly participates in various sensorimotor functions (visuospatial or reaction time tasks) and cognitive tasks involving striatal-cortical interactions. As discussed herein, while each of the midline and intralaminar nuclei are anatomically and functionally distinct, they collectively serve a vital role in several affective, cognitive and executive behaviors – as major components of a brainstem-diencephalic-thalamocortical circuitry.

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Optogenetic perturbation of projections from thalamic nucleus reuniens to hippocampus disrupts spatial working memory retrieval more than encoding

Cited by 9 publications

References 28 publications

Altered theta rhythm and hippocampal-cortical interactions underlie working memory deficits in a hyperglycemia risk factor model of Alzheimer’s disease

Altered theta rhythm and hippocampal-cortical interactions underlie working memory deficits in a hyperglycemia risk factor model of Alzheimer’s disease

Dependence of Working Memory on Coordinated Activity Across Brain Areas

Structural and functional organization of the midline and intralaminar nuclei of the thalamus

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