scholarly journals Long-term synaptic plasticity in hippocampal neurogliaform interneurons

2019 ◽  
Author(s):  
Marion S. Mercier ◽  
Vincent Magloire ◽  
Jonathan Cornford ◽  
Dimitri M. Kullmann
Keyword(s):  
Entorhinal Cortex ◽  
Pyramidal Cells ◽  
Long Term Potentiation ◽  
Stratum Radiatum ◽  
Dependent Manner ◽  
Feed Forward ◽  
Term Potentiation ◽  
Feed Forward Inhibition ◽  
Stimulation Of

AbstractHippocampal interneurons located within stratum lacunosum-moleculare (SLM), which include neurogliaform (NGF) cells, mediate powerful feed-forward inhibition that can modulate spiking and plasticity in CA1 pyramidal cells. Despite evidence of long-term plasticity at excitatory inputs onto almost all other hippocampal interneuron subtypes, including stratum radiatum feed-forward interneurons, it is not known whether long-term potentiation (LTP) occurs in CA1 SLM interneurons. Here, we show that these interneurons exhibit Hebbian NMDA receptor-dependent LTP, and that Ca2+ influx through voltage-gated Ca2+ channels can also be sufficient for induction of plasticity. Furthermore, using an optogenetic dissection strategy, we find that selective stimulation of excitatory fibers from entorhinal cortex can induce LTP in SLM interneurons, whilst stimulation of thalamic afferents from the nucleus reuniens, also known to project to SLM, does not. Finally, we show that a mouse line selective for cortical NGF cells, where Cre recombinase is under the control of the neuron-derived neurotrophic factor (NDNF) promoter, can also be used to target these interneurons within the hippocampus, and that hippocampal NGF cells exhibit LTP. Recruitment of NGF cells can thus be persistently enhanced in an activity-dependent manner, implying that their role in gating dendritic signaling in pyramidal neurons is modifiable.Significance statementLong-term potentiation (LTP) of synaptic transmission within the hippocampus is involved in memory formation and spatial navigation. While LTP has been extensively studied in excitatory principal cells, less is known about plasticity mechanisms in inhibitory interneurons, which represent a diverse population of cells. Here we characterize LTP in interneurons that mediate powerful feed-forward inhibition of pyramidal neuron distal dendrites, and show that this plasticity can be induced by afferents originating in the entorhinal cortex. Importantly, we identify at least a subset of these LTP-expressing interneurons as neurogliaform cells. The results shed light on this relatively understudied sub-type of hippocampal interneurons and show that their recruitment by extrinsic afferents can be modified in a use-dependent manner.

2-Deoxyglucose–Induced Long-Term Potentiation in CA1 Is Not Prevented by Intraneuronal Chelator

2000 ◽  
Vol 83 (1) ◽  
pp. 177-180 ◽  
Author(s):  
Yong-Tao Zhao ◽  
Krešimir Krnjević
Keyword(s):  
Ethylene Glycol ◽  
Hippocampal Slices ◽  
Long Term Potentiation ◽  
Stratum Radiatum ◽  
Tetanic Stimulation ◽  
Tetraacetic Acid ◽  
Ca1 Neurons ◽  
Term Potentiation ◽  
Stimulation Of

In hippocampal slices, temporary (10–20 min) replacement of glucose with 10 mM 2-deoxyglucose is followed by marked and very sustained potentiation of EPSPs (2-DG LTP). To investigate its mechanism, we examined 2-DG's effect in CA1 neurons recorded with sharp 3 M KCl electrodes containing a strong chelator, 50 or 100 mM ethylene glycol-bis(β-aminoethyl ether)- N, N, N′, N′-tetraacetic acid (EGTA). In most cases, field EPSPs were simultaneously recorded and conventional LTP was also elicited in some cells by tetanic stimulation of stratum radiatum. 2-DG potentiated intracellular EPSP slopes by 48 ± 5.1% (SE) in nine cells recorded with plain KCl electrodes and by 52 ± 6.2% in seven cells recorded with EGTA-containing electrodes. In four of the latter cells, tetanic stimulation (twice 100 Hz for 1 s) failed to evoke LTP (2 ± 1.1%), although field EPSPs were clearly potentiated (by 28 ± 6.9%). Thus unlike tetanic LTP, 2-DG LTP is not readily prevented by postsynaptic intraneuronal injection of EGTA. These findings agree with other evidence that the rise in postsynaptic (somatic) [Ca2+]i caused by 2-DG is not the principal trigger for the subsequent 2-DG LTP and that it may be a purely presynaptic phenomenon.

The involvement of nonspiking cells in long-term potentiation of synaptic transmission in the hippocampus

1988 ◽  
Vol 66 (6) ◽  
pp. 841-844 ◽  
Author(s):  
B. R. Sastry ◽  
J. W. Goh ◽  
P. B. Y. May ◽  
S. S. Chirwa
Keyword(s):  
Pyramidal Neurons ◽  
Hippocampal Slices ◽  
Long Term Potentiation ◽  
Stratum Radiatum ◽  
Ca1 Pyramidal Neurons ◽  
Term Potentiation ◽  
Ca1 Area ◽  
Glial Depolarization ◽  
Stimulation Of

In guinea pig hippocampal slices, stimulation of stratum radiatum during depolarization (with intracellular current injections) of nonspiking cells (presumed to be glia) in the apical dendritic area of CA1 pyramidal neurons resulted in a subsequent long-term potentiation of intracellularly recorded excitatory postsynaptic potentials as well as extracellularly recorded population spikes in the CA1 area. Tetanic stimulation of stratum radiatum resulted in a subsequent prolonged depolarization of the presumed glial cells, and this depolarization was smaller when the tetanus was given during the presence of 2-amino-5-phosphonovalerate or when the slices were exposed to Ca2+-free medium containing Mn2+ and Mg2+. These results suggest that glial depolarization is involved as one of the steps in generating long-term potentiation.

Evoked potentials and long-term potentiation in the mouse dentate gyrus after stimulation of the entorhinal cortex

1982 ◽  
Vol 75 (1) ◽  
pp. 134-148 ◽  
Author(s):  
Kathy Payne ◽  
Charles J. Wilson ◽  
Stephen Young ◽  
Eva Fifkova ◽  
Philip M. Groves
Keyword(s):  
Evoked Potentials ◽  
Dentate Gyrus ◽  
Entorhinal Cortex ◽  
Long Term Potentiation ◽  
Term Potentiation ◽  
Stimulation Of

scholarly journals Effect of Prenatal Protein Malnutrition on Long-Term Potentiation and BDNF Protein Expression in the Rat Entorhinal Cortex after Neocortical and Hippocampal Tetanization

2008 ◽  
Vol 2008 ◽  
pp. 1-9 ◽  
Author(s):  
Alejandro Hernández ◽  
Héctor Burgos ◽  
Mauricio Mondaca ◽  
Rafael Barra ◽  
Héctor Núñez ◽  
...  
Keyword(s):  
Entorhinal Cortex ◽  
Memory Performance ◽  
Occipital Cortex ◽  
Long Term Potentiation ◽  
Learning Performance ◽  
Pregnant Rats ◽  
Maternal Malnutrition ◽  
Term Potentiation ◽  
Stimulation Of

Reduction of the protein content from 25 to 8% casein in the diet of pregnant rats results in impaired neocortical long-term potentiation (LTP) of the offspring together with lower visuospatial memory performance. The present study was aimed to investigate whether this type of maternal malnutrition could result in modification of plastic capabilities of the entorhinal cortex (EC) in the adult progeny. Unlike normal eutrophic controls, 55–60-day-old prenatally malnourished rats were unable to develop LTP in the medial EC to tetanizing stimulation delivered to either the ipsilateral occipital cortex or the CA1 hippocampal region. Tetanizing stimulation of CA1 also failed to increase the concentration of brain-derived neurotrophic factor (BDNF) in the EC of malnourished rats. Impaired capacity of the EC of prenatally malnourished rats to develop LTP and to increase BDNF levels during adulthood may be an important factor contributing to deficits in learning performance having adult prenatally malnourished animals.

Field potential evidence for long-term potentiation of feed-forward inhibition in the rat dentate gyrus

1987 ◽  
Vol 401 (1) ◽  
pp. 87-94 ◽  
Author(s):  
Edward W. Kairiss ◽  
Wickliffe C. Abraham ◽  
David K. Bilkey ◽  
Graham V. Goddard
Keyword(s):  
Dentate Gyrus ◽  
Field Potential ◽  
Long Term Potentiation ◽  
Feed Forward ◽  
Term Potentiation ◽  
Feed Forward Inhibition

Protein kinase C injection into hippocampal pyramidal cells elicits features of long term potentiation

Nature ◽  
1987 ◽  
Vol 328 (6129) ◽  
pp. 426-429 ◽  
Author(s):  
G.-Y. Hu ◽  
Ø. Hvalby ◽  
S. I. Walaas ◽  
K. A. Albert ◽  
P. Skjeflo ◽  
...  
Keyword(s):  
Protein Kinase C ◽  
Protein Kinase ◽  
Pyramidal Cells ◽  
Long Term Potentiation ◽  
Kinase C ◽  
Term Potentiation ◽  
Hippocampal Pyramidal Cells

Induction of long-term potentiation without participation of N-methyl-D-aspartate receptors in kitten visual cortex

1991 ◽  
Vol 65 (1) ◽  
pp. 20-32 ◽  
Author(s):  
Y. Komatsu ◽  
S. Nakajima ◽  
K. Toyama
Keyword(s):  
Nmda Receptors ◽  
Stimulus Frequency ◽  
Low Frequency ◽  
Nmda Antagonist ◽  
Long Term Potentiation ◽  
Conditioning Stimulation ◽  
Postsynaptic Potential ◽  
Term Potentiation ◽  
Stimulation Of

1. Intracellular recording was made from layer II-III cells in slice preparations of kitten (30-40 days old) visual cortex. Low-frequency (0.1 Hz) stimulation of white matter (WM) usually evoked an excitatory postsynaptic potential (EPSP) followed by an inhibitory postsynaptic potential (IPSP). The postsynaptic potentials (PSPs) showed strong dependence on stimulus frequency. Early component of EPSP and IPSP evoked by weak stimulation both decreased monotonically at frequencies greater than 0.5-1 Hz. Strong stimulation similarly depressed the early EPSP at higher frequencies (greater than 2 Hz) and replaced the IPSP with a late EPSP, which had a maximum amplitude in the stimulus frequency range of 2-5 Hz. 2. Very weak WM stimulation sometimes evoked EPSPs in isolation from IPSPs. The falling phase of the EPSP revealed voltage dependence characteristic to the responses mediated by N-methyl-D-aspartate (NMDA) receptors and was depressed by application of an NMDA antagonist DL-2-amino-5-phosphonovalerate (APV), whereas the rising phase of the EPSP was insensitive to APV. 3. The early EPSPs followed by IPSPs were insensitive to APV but were replaced with a slow depolarizing potential by application of a non-NMDA antagonist 6,7-dinitro-quinoxaline-2,3-dione (DNQX), indicating that the early EPSP is mediated by non-NMDA receptors. The slow depolarization was mediated by NMDA receptors because it was depressed by membrane hyperpolarization or addition of APV. 4. The late EPSP evoked by higher-frequency stimulation was abolished by APV, indicating that it is mediated by NMDA receptors, which are located either on the recorded cell or on presynaptic cells to the recorded cells. 5. Long-term potentiation (LTP) of EPSPs was examined in cells perfused with solutions containing 1 microM bicuculline methiodide (BIM), a gamma-aminobutyric acid (GABA) antagonist. WM was stimulated at 2 Hz for 15 min as a conditioning stimulus to induce LTP, and the resultant changes were tested by low-frequency (0.1 Hz) stimulation of WM. 6. LTP of early EPSPs occurred in more than one-half of the cells (8/13) after strong conditioning stimulation. The rising slope of the EPSP was increased 1.6 times on average. 7. To test involvement of NMDA receptors in the induction of LTP in the early EPSP, the effect of conditioning stimulation was studied in a solution containing 100 microM APV, which was sufficient to block completely synaptic transmission mediated by NMDA receptors. LTP occurred in the same frequency and magnitude as in control solution.

scholarly journals Imaging spatio-temporal patterns of long-term potentiation in mouse hippocampus

2003 ◽  
Vol 358 (1432) ◽  
pp. 689-693 ◽  
Author(s):  
Toshiyuki Hosokawa ◽  
Masaki Ohta ◽  
Takeshi Saito ◽  
Alan Fine
Keyword(s):  
Hippocampal Slices ◽  
Temporal Patterns ◽  
Long Term Potentiation ◽  
Optical Recording ◽  
Stratum Radiatum ◽  
High Frequency Stimulation ◽  
Optical Signals ◽  
Term Potentiation ◽  
Spatio Temporal

Spatio-temporal patterns of neuronal activity before and after the induction of long-term potentiation in mouse hippocampal slices were studied using a real-time high-resolution optical recording system. After staining the slices with voltage-sensitive dye, transmitted light images and extracellular field potentials were recorded in response to stimuli applied to CA1 stratum radiatum. Optical and electrical signals in response to single test pulses were enhanced for at least 30 minutes after brief high-frequency stimulation at the same site. In two-pathway experiments, potentiation was restricted to the tetanized pathway. The optical signals demonstrated that both the amplitude and area of the synaptic response were increased, in patterns not predictable from the initial, pretetanus, pattern of activation. Optical signals will be useful for investigating spatio-temporal patterns of synaptic enhancement underlying information storage in the brain.

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