Hippocampal area CA2: properties and contribution to hippocampal function

Robert, Valérie; Cassim, Sadiyah; Chevaleyre, Vivien; Piskorowski, Rebecca A.

doi:10.1007/s00441-017-2769-7

Cited by 17 publications

(9 citation statements)

References 103 publications

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“…Major questions remain concerning how social information is encoded by the hippocampus and the precise role of area CA2 in this process. During social exploration, CA2 PNs likely receive theta-locked inputs from the entorhinal cortex, the septum, the supramammillary nucleus, and area CA3 (Robert et al, 2018). Our results indicate that changes in the V M resulting from M1 and M3 activation in high cholinergic tone suppress CA3 inputs more than cortical inputs, as has been observed in other CA regions (Kremin and Hasselmo, 2007; Hasselmo and Schnell, 1994).…”

Section: Discussionmentioning

confidence: 99%

The mechanisms shaping CA2 pyramidal neuron action potential bursting induced by muscarinic acetylcholine receptor activation

Robert

Therreau

Davatolhagh

et al. 2020

Journal of General Physiology

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Recent studies have revealed that hippocampal area CA2 plays an important role in hippocampal network function. Disruption of this region has been implicated in neuropsychiatric disorders. It is well appreciated that cholinergic input to the hippocampus plays an important role in learning and memory. While the effect of elevated cholinergic tone has been well studied in areas CA1 and CA3, it remains unclear how changes in cholinergic tone impact synaptic transmission and the intrinsic properties of neurons in area CA2. In this study, we applied the cholinergic agonist carbachol and performed on-cell, whole-cell, and extracellular recordings in area CA2. We observed that under conditions of high cholinergic tone, CA2 pyramidal neurons depolarized and rhythmically fired bursts of action potentials. This depolarization depended on the activation of M1 and M3 cholinergic receptors. Furthermore, we examined how the intrinsic properties and action-potential firing were altered in CA2 pyramidal neurons treated with 10 µM carbachol. While this intrinsic burst firing persisted in the absence of synaptic transmission, bursts were shaped by synaptic inputs in the intact network. We found that both excitatory and inhibitory synaptic transmission were reduced upon carbachol treatment. Finally, we examined the contribution of different channels to the cholinergic-induced changes in neuronal properties. We found that a conductance from Kv7 channels partially contributed to carbachol-induced changes in resting membrane potential and membrane resistance. We also found that D-type potassium currents contributed to controlling several properties of the bursts, including firing rate and burst kinetics. Furthermore, we determined that T-type calcium channels and small conductance calcium-activated potassium channels play a role in regulating bursting activity.

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Section: Discussionmentioning

confidence: 99%

The mechanisms shaping CA2 pyramidal neuron action potential bursting induced by muscarinic acetylcholine receptor activation

Robert

Therreau

Davatolhagh

et al. 2020

Journal of General Physiology

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“…Synaptic plasticity in the trisynaptic pathway is thought to be the underlying basis of hippocampal-dependent memory [60,61] and has received much attention since its initial discovery. However, the importance of area CA2 in relation to hippocampal function, physiology, and behavior has only recently been investigated [62][63][64][65][66].…”

Section: Rgs14 In the Hippocampusmentioning

confidence: 99%

RGS14 Regulation of Post-Synaptic Signaling and Spine Plasticity in Brain

Harbin

Bramlett

Montañez-Miranda

et al. 2021

IJMS

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The regulator of G-protein signaling 14 (RGS14) is a multifunctional signaling protein that regulates post synaptic plasticity in neurons. RGS14 is expressed in the brain regions essential for learning, memory, emotion, and stimulus-induced behaviors, including the basal ganglia, limbic system, and cortex. Behaviorally, RGS14 regulates spatial and object memory, female-specific responses to cued fear conditioning, and environmental- and psychostimulant-induced locomotion. At the cellular level, RGS14 acts as a scaffolding protein that integrates G protein, Ras/ERK, and calcium/calmodulin signaling pathways essential for spine plasticity and cell signaling, allowing RGS14 to naturally suppress long-term potentiation (LTP) and structural plasticity in hippocampal area CA2 pyramidal cells. Recent proteomics findings indicate that RGS14 also engages the actomyosin system in the brain, perhaps to impact spine morphogenesis. Of note, RGS14 is also a nucleocytoplasmic shuttling protein, where its role in the nucleus remains uncertain. Balanced nuclear import/export and dendritic spine localization are likely essential for RGS14 neuronal functions as a regulator of synaptic plasticity. Supporting this idea, human genetic variants disrupting RGS14 localization also disrupt RGS14’s effects on plasticity. This review will focus on the known and unexplored roles of RGS14 in cell signaling, physiology, disease and behavior.

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“…In examining neural firing in the hippocampus of subjects in a maze, we found neural firing that could not be classified as either of the locomotor or SWR states (Figures and ; Kay et al, ). This activity was most clearly distinguished from locomotor and SWR activity by virtue of a distinct population of neurons located in subregion CA2, an understudied subregion of the hippocampus (itself the focus of recent reviews, Jones & McHugh, ; Dudek, Alexander, & Farris, ; Robert, Cassim, Chevaleyre, & Piskorowski, ).…”

Section: Three Brain States In the Hippocampusmentioning

confidence: 99%

Three brain states in the hippocampus and cortex

Kay

Frank

2019

Hippocampus

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Contemporary brain research seeks to understand how cognition is reducible to neural activity. Crucially, much of this effort is guided by a scientific paradigm that views neural activity as essentially driven by external stimuli. In contrast, recent perspectives argue that this paradigm is by itself inadequate, and that understanding patterns of activity intrinsic to the brain is needed to explain cognition. Yet despite this critique, the stimulus-driven paradigm still dominates - possibly because a convincing alternative has not been clear. Here we review a series of experimental findings in the hippocampus suggesting such an alternative. These findings indicate that hippocampal neural activity occurs in one of three brain states that have radically different anatomical, physiological, representational, and behavioral correlates, together implying different roles in cognition. This three-state framework also indicates that hippocampal neural representations follow a surprising pattern of organization at the timescale of ∼1 s or longer. Lastly, beyond the hippocampus, recent breakthroughs indicate three parallel states in cortex, suggesting shared principles and brain-wide organization of intrinsic neural activity. This article is protected by copyright. All rights reserved.

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Hippocampal area CA2: properties and contribution to hippocampal function

Cited by 17 publications

References 103 publications

The mechanisms shaping CA2 pyramidal neuron action potential bursting induced by muscarinic acetylcholine receptor activation

The mechanisms shaping CA2 pyramidal neuron action potential bursting induced by muscarinic acetylcholine receptor activation

RGS14 Regulation of Post-Synaptic Signaling and Spine Plasticity in Brain

Three brain states in the hippocampus and cortex

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