scholarly journals Long-term potentiation at pyramidal cell to somatostatin interneuron synapses controls hippocampal network plasticity and memory

2021 ◽  
Author(s):  
Jean-Claude Lacaille ◽  
Azam Asgarihafshejani ◽  
Eve Honore ◽  
Francois-Xavier Michon ◽  
Isabel Laplante
Keyword(s):  
Pyramidal Cell ◽  
Memory Consolidation ◽  
Pyramidal Cells ◽  
Long Term Potentiation ◽  
Feedback Mechanism ◽  
Ca1 Pyramidal Cells ◽  
Term Potentiation ◽  
Hippocampal Network

Hippocampal somatostatin (SOM) cells are dendrite-projecting inhibitory interneurons. CA1 SOM cells receive major excitatory inputs from pyramidal cells (PC-SOM synapses) which show mGluR1a- and mTORC1-mediated long-term potentiation (LTP). PC-SOM synapse LTP contributes to CA1 network metaplasticity and memory consolidation, but whether it is sufficient to regulate these processes remains unknown. Here we used optogenetic stimulation of CA1 pyramidal cells and whole cell recordings in slices to show that optogenetic theta burst stimulation (TBSopto) produces LTP at PC-SOM synapses. At the network level, we found that TBSopto differentially regulates metaplasticity of pyramidal cell inputs: enhancing LTP at Schaffer collateral synapses and depressing LTP at temporo-ammonic synapses. At the behavioral level, we uncovered that in vivo TBSopto regulates learning-induced LTP at PC-SOM synapses, as well as contextual fear memory. Thus, LTP of PC-SOM synapses is a long-term feedback mechanism controlling pyramidal cell synaptic plasticity, sufficient to regulate memory consolidation.

scholarly journals Aη-α and Aη-β peptides impair LTP ex vivo within the low nanomolar range and impact neuronal activity in vivo

2021 ◽  
Vol 13 (1) ◽  
Author(s):  
Maria Mensch ◽  
Jade Dunot ◽  
Sandy M. Yishan ◽  
Samuel S. Harris ◽  
Aline Blistein ◽  
...  
Keyword(s):  
Neuronal Activity ◽  
Ex Vivo ◽  
Long Term Potentiation ◽  
Network Activity ◽  
Strongly Correlated ◽  
App Processing ◽  
Term Potentiation ◽  
Hippocampal Network

Abstract Background Amyloid precursor protein (APP) processing is central to Alzheimer’s disease (AD) etiology. As early cognitive alterations in AD are strongly correlated to abnormal information processing due to increasing synaptic impairment, it is crucial to characterize how peptides generated through APP cleavage modulate synapse function. We previously described a novel APP processing pathway producing η-secretase-derived peptides (Aη) and revealed that Aη–α, the longest form of Aη produced by η-secretase and α-secretase cleavage, impaired hippocampal long-term potentiation (LTP) ex vivo and neuronal activity in vivo. Methods With the intention of going beyond this initial observation, we performed a comprehensive analysis to further characterize the effects of both Aη-α and the shorter Aη-β peptide on hippocampus function using ex vivo field electrophysiology, in vivo multiphoton calcium imaging, and in vivo electrophysiology. Results We demonstrate that both synthetic peptides acutely impair LTP at low nanomolar concentrations ex vivo and reveal the N-terminus to be a primary site of activity. We further show that Aη-β, like Aη–α, inhibits neuronal activity in vivo and provide confirmation of LTP impairment by Aη–α in vivo. Conclusions These results provide novel insights into the functional role of the recently discovered η-secretase-derived products and suggest that Aη peptides represent important, pathophysiologically relevant, modulators of hippocampal network activity, with profound implications for APP-targeting therapeutic strategies in AD.

scholarly journals Selective Induction of LTP and LTD by Postsynaptic [Ca2+]i Elevation

1999 ◽  
Vol 81 (2) ◽  
pp. 781-787 ◽  
Author(s):  
Shao-Nian Yang ◽  
Yun-Gui Tang ◽  
Robert S. Zucker
Keyword(s):  
Calcium Concentration ◽  
Pyramidal Cells ◽  
Long Term Potentiation ◽  
Biological Information ◽  
Synaptic Modulation ◽  
Ca1 Pyramidal Cells ◽  
Caged Calcium ◽  
Term Potentiation ◽  
Calcium Compound

Selective Induction of LTP and LTD by Postsynaptic [Ca2+]i Elevation. Long-term potentiation (LTP) and long-term depression (LTD), two prominent forms of synaptic plasticity at glutamatergic afferents to CA1 hippocampal pyramidal cells, are both triggered by the elevation of postsynaptic intracellular calcium concentration ([Ca2+]i). To understand how one signaling molecule can be responsible for triggering two opposing forms of synaptic modulation, different postsynaptic [Ca2+]i elevation patterns were generated by a new caged calcium compound nitrophenyl-ethylene glycol-bis(β-aminoethyl ether)- N, N, N′, N′-tetraacetic acid in CA1 pyramidal cells. We found that specific patterns of [Ca2+]i elevation selectively activate LTP or LTD. In particular, only LTP was triggered by a brief increase of [Ca2+]i with relatively high magnitude, which mimics the [Ca2+]i rise during electrical stimulation typically used to induce LTP. In contrast, a prolonged modest rise of [Ca2+]i reliably induced LTD. An important implication of the results is that both the amplitude and the duration of an intracellular chemical signal can carry significant biological information.

scholarly journals Long-term potentiation at single fiber inputs to hippocampal CA1 pyramidal cells.

1996 ◽  
Vol 93 (16) ◽  
pp. 8710-8715 ◽  
Author(s):  
J. T. Isaac ◽  
G. O. Hjelmstad ◽  
R. A. Nicoll ◽  
R. C. Malenka
Keyword(s):  
Pyramidal Cells ◽  
Long Term Potentiation ◽  
Single Fiber ◽  
Ca1 Pyramidal Cells ◽  
Term Potentiation ◽  
Hippocampal Ca1

In Vitro Plasticity of the Direct Feedback Pathway in the Electrosensory System of Apteronotus leptorhynchus

1997 ◽  
Vol 78 (4) ◽  
pp. 1882-1889 ◽  
Author(s):  
Daliang Wang ◽  
Leonard Maler
Keyword(s):  
Pyramidal Cells ◽  
Long Term Potentiation ◽  
Tetanic Stimulation ◽  
Apteronotus Leptorhynchus ◽  
Term Potentiation ◽  
Direct Feedback ◽  
Feedback Pathway

Wang, Daliang and Leonard Maler. In vitro plasticity of the direct feedback pathway in the electrosensory system of Apteronotus leptorhynchus. J. Neurophysiol. 78: 1882–1889, 1997. We have used field and intracellular recording from pyramidal cells in an in vitro preparation of the electrosensory lateral line lobe (ELL) of Apteronotus leptorhynchus to investigate synaptic plasticity of a direct feedback pathway: the (StF). Tetanic stimulation of the StF enhanced the StF-evoked synaptic response by 145% in field and the excitatory postsynaptic potential (EPSP) 190% in intracellular recordings. Maximal enhancement occurred at 5 s and lasted for ∼120 s. Tetanic frequencies of 100–300 Hz produced enhancement; lower or higher frequencies failed to produce statistically significant changes in EPSP amplitude. Rates of 100–200 Hz occur in vivo in the cells of origin of the StF, suggesting that this form of plasticity may be operative under natural conditions. We could not elicit either long-term potentiation or depression by any stimulation protocol of the StF; in the case of long-term potentiation, this held even when excitatory transmission was enhanced by application of bicuculline, a γ-aminobutyric acid-A antagonist. When tetanic stimulation of the StF was paired with hyperpolarization of pyramidal cells, subsequent StF-evoked EPSPs were increased by 146% (5 min posttetanus); this anti-Hebbian synaptic enhancement lasted for ∼10 min. Neither tetanic stimulation alone, hyperpolarization alone, nor tetanic stimulation paired with pyramidal cell depolarization altered StF-evoked EPSP amplitudes on this time scale. Anti-Hebbian synaptic enhancement was not blocked by the N-methyl-d-aspartate–receptor antagonist D.L-aminophosphovalerate. The in vitro demonstration of anti-Hebbian plasticity at StF synapses replicates similar in vivo results. Anti-Hebbian synaptic plasticity of the StF may be responsible in part for the ability of gymnotiform fish to reject redundant electrosensory signals.

Long-term potentiation at the apical and basal dendritic synapses of CA1 after local stimulation in behaving rats

1995 ◽  
Vol 73 (5) ◽  
pp. 1938-1946 ◽  
Author(s):  
L. S. Leung ◽  
B. Shen
Keyword(s):  
High Frequency ◽  
Pyramidal Cells ◽  
Long Term Potentiation ◽  
Ca1 Pyramidal Cells ◽  
Stratum Oriens ◽  
Term Potentiation ◽  
Theta Frequency ◽  
Freely Behaving ◽  
Local Stimulation

1. We recorded the extracellular excitatory postsynaptic potentials (EPSPs) in CA1 in the freely behaving rats after stimulation of the apical dendritic and basal dendritic afferents. The apical dendritic population EPSP was negative at the apical dendritic layers and positive at stratum oriens and alveus. The basal dendritic population EPSP was negative at basal dendritic layer (stratum oriens) and positive at the cell body and apical dendritic layers. 2. We delivered various tetanic stimulus patterns in an attempt to elicit long-term potentiation (LTP) at the apical dendritic synapse of CA1 pyramidal cells. A 200-Hz high-frequency train (HF) 1 s in duration was more successful than theta-frequency primed bursts (PBs; 1 or 4 priming pulses followed by 10 or 4 pulses at 100 Hz) in eliciting LTP of the apical dendritic population EPSP, recorded either ipsilaterally or contralaterally. 3. Tetanus applied to the apical dendritic afferents occasionally elicited long-term depression (LTD) at an intensity lower than the LTP threshold. LTD persisted to > or = 1 day after a tetanus. 4. High-intensity tetanic stimulations often elicited hippocampal afterdischarges (ADs). If the AD duration was brief (< 15 s), apical dendritic LTP could follow the AD. However, if the AD duration was long, no apical dendritic LTP was observed. Tetanus that evoked an apical dendritic LTP typically evoked a short hippocampal AD < 15 s in duration. 5. LTP of the basal dendritic population EPSP was readily elicited either after an HF or a PB tetanus of low (1.5-2 times threshold) stimulus intensity.(ABSTRACT TRUNCATED AT 250 WORDS)

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