Top-down control of hippocampal signal-to-noise by prefrontal long-range inhibition

Malik, Ruchi; Li, Yang; Schamiloglu, Selin; Sohal, Vikaas S.

doi:10.1016/j.cell.2022.04.001

Cited by 71 publications

(75 citation statements)

References 95 publications

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“…This work reveals that the retrieval of fear extinction is associated with top-down theta synchrony such that mPFC leads dHPC theta. Although it has long been assumed that the mPFC does not project to the dHPC (Vertes et al, 2007), a recent report discovered for the first time that a population of mPFC longrange inhibitory neurons directly project to the dHPC and play a critical role in increasing hippocampal signal-to-noise ratio for spatial encoding by driving feedforward inhibition and increasing mPFC-dHPC gamma synchrony (Malik et al, 2022). Conversely, the mPFC has been proposed to interface with the dHPC via a disynaptic circuit through the nucleus reuniens of the thalamus (Vertes et al, 2007;Jin and Maren, 2015), which is also critical to fear extinction (Ramanathan et al, 2018a,b).…”

Section: Prefrontal Top-down Theta Synchrony Regulates Fear Extinctionmentioning

confidence: 99%

Neural Oscillations in Aversively Motivated Behavior

Totty

Maren²

2022

Front. Behav. Neurosci.

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Fear and anxiety-based disorders are highly debilitating and among the most prevalent psychiatric disorders. These disorders are associated with abnormal network oscillations in the brain, yet a comprehensive understanding of the role of network oscillations in the regulation of aversively motivated behavior is lacking. In this review, we examine the oscillatory correlates of fear and anxiety with a particular focus on rhythms in the theta and gamma-range. First, we describe neural oscillations and their link to neural function by detailing the role of well-studied theta and gamma rhythms to spatial and memory functions of the hippocampus. We then describe how theta and gamma oscillations act to synchronize brain structures to guide adaptive fear and anxiety-like behavior. In short, that hippocampal network oscillations act to integrate spatial information with motivationally salient information from the amygdala during states of anxiety before routing this information via theta oscillations to appropriate target regions, such as the prefrontal cortex. Moreover, theta and gamma oscillations develop in the amygdala and neocortical areas during the encoding of fear memories, and interregional synchronization reflects the retrieval of both recent and remotely encoded fear memories. Finally, we argue that the thalamic nucleus reuniens represents a key node synchronizing prefrontal-hippocampal theta dynamics for the retrieval of episodic extinction memories in the hippocampus.

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Section: Prefrontal Top-down Theta Synchrony Regulates Fear Extinctionmentioning

confidence: 99%

Neural Oscillations in Aversively Motivated Behavior

Totty

Maren²

2022

Front. Behav. Neurosci.

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Section: Introductionmentioning

confidence: 99%

“…Anatomically, higher-order thalamocortical connections through the nucleus reuniens likely contribute to controlling these memory dynamics (Gazzaley and D’Esposito, 2007; Theyel, Llano and Sherman, 2010; Poulet et al ., 2012; Ito et al ., 2015; Viena, Linley and Vertes, 2018; Jayachandran et al ., 2019; Malik et al ., 2022). While, the hippocampus directly projects to the prefrontal cortex (Hoover and Vertes, 2007), only sparse return projections have been identified (Sesack et al ., 1989; Laroche, Davis and Jay, 2000; Rajasethupathy et al ., 2015; Malik et al ., 2022). Instead, memory-related interactions depend on the nucleus reuniens, a region of the midline thalamus that provides a bi-directional control over prefrontal-hippocampal loops (Vertes et al ., 2006; Varela et al ., 2014; Dolleman-van der Weel et al ., 2019; Viena, Vertes and Linley, 2021).…”

Section: Introductionmentioning

confidence: 99%

Reuniens transiently synchronizes memory networks at beta frequencies

Jayachandran

Viena

Garcia

et al. 2022

Preprint

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Using episodic memories to help guide decisions requires top-down medial prefrontal cortex interactions with the hippocampus. Mechanistically, this integrated prefrontal-hippocampal memory state is thought to be organized by synchronized network oscillations and mediated by connectivity with the nucleus reuniens of the thalamus. Here, we recorded local field potentials from the prefrontal-reuniens-hippocampal network while rats were engaged in a nonspatial sequence memory task which helps isolate memory-related activity from running-related oscillations. We found that synchronous prefrontal-hippocampal beta bursts (15-30 Hz) were dominant during memory trials, whereas synchronous theta (6-12 Hz) was highest during running. Beta rose during a trial and peaked just before a decision, whereas theta was highest during running. Beta bursts first appeared in reuniens and then in prefrontal and hippocampal sites simultaneously, suggesting beta could be directly driven by reuniens. To test this, we used an optogenetic approach (retroAAV-ChR2) to see if reuniens was capable of driving prefrontal-hippocampal beta synchrony. Reuniens activation induced prefrontal-hippocampal beta coherence, and reduced theta coherence, resembling the observed memory-driven network state. These findings demonstrate for the first time that reuniens contributes to memory by driving transient synchronous beta in the prefrontal-hippocampal system facilitating coherent interactions that sub-serve memory-based decision making.

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“…The formation and consolidation of spatial memories requires additional hippocampal and mPFC interplay through VIP + neurons (Maviel et al (2004), Lee et al (2019), Malik et al (2022)).…”

Section: Impairments In Spatial Learning and Memorymentioning

confidence: 99%

Loss of GABA co-transmission from cholinergic neurons impairs behaviors related to hippocampal, striatal, and medial prefrontal cortex functions

Goral

Harper

Bernstein

et al. 2022

Preprint

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Altered signaling or function of acetylcholine (ACh) has been reported in various neurological diseases, including Alzheimer's disease, Tourette syndrome, epilepsy among others. Many neurons that release ACh also co-transmit the neurotransmitter gamma-aminobutyrate (GABA) at synapses in the hippocampus, striatum, and medial prefrontal cortex (mPFC). Although ACh transmission is crucial for higher brain functions such as learning and memory, the role of co-transmitted GABA from ACh neurons in brain function remains unknown. Thus, the overarching goal of this study was to investigate how a systemic loss of GABA co-transmission from ACh neurons affected the behavioral performance of mice. To do this, we used a conditional knock-out mouse of the vesicular GABA transporter (vGAT) crossed with the ChAT-Cre driver line to selectively ablate GABA co-transmission at ACh synapses. In a comprehensive series of standardized behavioral assays, we compared Cre-negative control mice with Cre-positive vGAT knock-out mice of both sexes. Loss of GABA co-transmission from ACh neurons did not disrupt the animal's sociability, motor skills or sensation. However, in the absence of GABA co-transmission, we found significant alterations in social, spatial and fear memory as well as a reduced reliance on striatum-dependent response strategies in a T-maze. In addition, male CKO mice showed increased locomotion. Taken together, the loss of GABA co-transmission leads to deficits in higher brain functions and behaviors. Therefore, we propose that ACh/GABA co-transmission modulates neural circuitry involved in the affected behaviors.

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Top-down control of hippocampal signal-to-noise by prefrontal long-range inhibition

Cited by 71 publications

References 95 publications

Neural Oscillations in Aversively Motivated Behavior

Neural Oscillations in Aversively Motivated Behavior

Reuniens transiently synchronizes memory networks at beta frequencies

Loss of GABA co-transmission from cholinergic neurons impairs behaviors related to hippocampal, striatal, and medial prefrontal cortex functions

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