scholarly journals Low-frequency stimulation induces long-term depression and slow onset long-term potentiation at perforant path-dentate gyrus synapses in vivo

2014 ◽  
Vol 111 (6) ◽  
pp. 1259-1273 ◽  
Author(s):  
Jossina Gonzalez ◽  
Isaiah S. Morales ◽  
Desiree M. Villarreal ◽  
Brian E. Derrick
Keyword(s):  
Nmda Receptor ◽  
Low Frequency ◽  
Perforant Path ◽  
Paired Pulse ◽  
Anesthetized Rats ◽  
Low Frequency Stimulation ◽  
Frequency Stimulation ◽  
Slow Onset

The expression of homosynaptic long-term depression (LTD) is thought to mediate a crucial role in sustaining memory function. Our in vivo investigations of LTD expression at lateral (LPP) and medial perforant path (MPP) synapses in the dentate gyrus (DG) corroborate prior demonstrations that PP-DG LTD is difficult to induce in intact animals. In freely moving animals, LTD expression occurred inconsistently among LPP-DG and MPP-DG responses. Interestingly, following acute electrode implantation in anesthetized rats, low-frequency stimulation (LFS; 900 pulses, 1 Hz) promotes slow-onset LTP at both MPP-DG and LPP-DG synapses that utilize distinct induction mechanisms. Systemic administration of the N-methyl-d-aspartate (NMDA) receptor antagonist (+/−)-cyclopiperidine-6-piperiperenzine (CPP; 10 mg/kg) 90 min before LFS selectively blocked MPP-DG but not LPP-DG slow onset LTP, suggesting MPP-DG synapses express a NMDA receptor-dependent slow onset LTP whereas LPP-DG slow onset LTP induction is NMDA receptor independent. In experiments where paired-pulse LFS (900 paired pulses, 200-ms paired-pulse interval) was used to induce LTD, paired-pulse LFS of the LPP resulted in rapid onset LTP of DG responses, whereas paired-pulse LFS of the MPP induced slow onset LTP of DG responses. Although LTD observations were very rare following acute electrode implantation in anesthetized rats, LPP-DG LTD was demonstrated in some anesthetized rats with previously implanted electrodes. Together, our data indicate in vivo PP-DG LTD expression is an inconsistent phenomenon that is primarily observed in recovered animals, suggesting perturbation of the dentate through surgery-related tissue trauma influences both LTD incidence and LTP induction at PP-DG synapses in vivo.

Long-Term Synaptic Plasticity in the Honeybee

1997 ◽  
Vol 78 (1) ◽  
pp. 528-532 ◽  
Author(s):  
S. Oleskevich ◽  
J. D. Clements ◽  
M. V. Srinivasan
Keyword(s):  
Synaptic Plasticity ◽  
Field Potential ◽  
Low Frequency ◽  
Fold Increase ◽  
Afferent Input ◽  
Insect Brain ◽  
Paired Pulse ◽  
Frequency Stimulation

Oleskevich, S., J. D. Clements, and M. V. Srinivasan. Long-term synaptic plasticity in the honeybee. J. Neurophysiol. 78: 528–532, 1997. A monosynaptic response was recorded in vivo in the mushroom body of the bee brain, an important site for memory consolidation. Focal electrical stimulation of a major afferent input evoked an extracellular field potential that consisted of a presynaptic fiber volley and a postsynaptic response. We report a long-lasting potentiation of the synaptic response (2.6-fold increase; ≤3.5 h). Potentiation of the response was induced by low-frequency stimulation (0.02–1.0 Hz), was input specific, and was maintained in the absence of stimulation. Paired-pulse facilitation of the response was converted to paired-pulse depression after potentiation, suggesting a presynaptic mechanism. This is the first demonstration of long-term synaptic plasticity in the insect brain.

NMDA Receptor-Dependent Long-Term Synaptic Depression in the Entorhinal Cortex In Vitro

2003 ◽  
Vol 89 (4) ◽  
pp. 2112-2119 ◽  
Author(s):  
Saı̈d Kourrich ◽  
C. Andrew Chapman
Keyword(s):  
Nmda Receptor ◽  
Receptor Antagonist ◽  
Entorhinal Cortex ◽  
Low Frequency ◽  
Synaptic Depression ◽  
Paired Pulse ◽  
Pulse Stimulation

The entorhinal cortex receives a large projection from the piriform (primary olfactory) cortex and, in turn, provides the hippocampal formation with most of its cortical sensory input. Synaptic plasticity in this pathway may therefore affect the processing of olfactory information and memory encoding. We have recently found that long-term synaptic depression (LTD) can be induced in this pathway in vivo by repetitive paired-pulse stimulation but not by low-frequency (1 Hz) stimulation with single pulses. Here, we have used field potential recordings to investigate the stimulation parameters and transmitter receptors required for the induction of LTD in the rat entorhinal cortex in vitro. The effectiveness of low-frequency stimulation (900 pulses at 1 or 5 Hz) and repeated delivery of pairs of stimulation pulses (30-ms interpulse interval) was assessed. Only repeated paired-pulse stimulation resulted in lasting LTD, and a low-intensity paired-pulse stimulation protocol that induces LTD in vivo was only effective in the presence of the GABAA receptor antagonist bicuculline (50 μM). LTD could also be induced in normal ACSF, however, by increasing the number of pulse-pairs delivered and by increasing the stimulation intensity during LTD induction. The induction of LTD was blocked by constant bath application of the N-methyl-d-aspartate (NMDA) glutamate receptor antagonist d-2-amino-5-phosphonovalerate (50 μM), indicating that LTD is dependent on NMDA receptor activation. However, LTD was not blocked by the group I/II mGluR antagonist (RS)-α-ethyl-4-carboxyphenylglycine (500 μM) or by bicuculline (50 μM). The induction of LTD in the entorhinal cortex in vitro is therefore dependent on intense stimulation that recruits activation of NMDA receptors, but does not require concurrent activation of mGluRs or inhibitory synaptic inputs.

Reversal of LTP in the Hippocampal Afferent Fiber System to the Prefrontal Cortex In Vivo With Low-Frequency Patterns of Stimulation That Do Not Produce LTD

1997 ◽  
Vol 78 (2) ◽  
pp. 1155-1160 ◽  
Author(s):  
F. Burette ◽  
T. M. Jay ◽  
S. Laroche
Keyword(s):  
Prefrontal Cortex ◽  
Afferent Fiber ◽  
Low Frequency ◽  
Long Term Potentiation ◽  
Negative Wave ◽  
Fiber System ◽  
Low Frequency Stimulation ◽  
Frequency Stimulation

Burette, F., T. M. Jay, and S. Laroche. Reversal of LTP in the hippocampal afferent fiber system to the prefrontal cortex in vivo with low-frequency patterns of stimulation that do not produce LTD. J. Neurophysiol. 78: 1155–1160, 1997. We examined the efficacy of several patterns of low-frequency stimulation for producing long-term depression (LTD) or depotentiation in the hippocampal fiber pathway to the prefrontal cortex in the anesthetized rat. Field potentials elicited by stimulation of the CA1/subicular region of the ventral hippocampus were recorded in the prelimbic area of the prefrontal cortex. We found no evidence that low-frequency trains (0.5–1 Hz), consisting of either single pulses, paired pulses (35-ms interpulse interval), or two-pulse bursts (5-ms interval), produce LTD in the prefrontal cortex. In contrast, all three stimulus protocols were found to induce a small-amplitude, persistent potentiation of the amplitude of the negative wave of the field response recorded in the prefrontal cortex. We also examined the ability of patterns of low-frequency stimulation to produce depotentiation of previously established long-term potentiation (LTP). Although low-frequency stimulation with single pulses or paired pulses was ineffective, we found that the two-pulse burst protocol selectively produced a rapid reversal of LTP in the hippocampo-prefrontal cortex pathway. Depotentiation is reversible and can be induced >2 h after the induction of LTP. Repeated trains failed to decrease the prefrontal cortex response below the original, unpotentiated level. These findings demonstrate the existence of a depotentiation mechanism that is capable of exerting powerful control over ongoing or recently induced synaptic plasticity in hippocampocortical connections in vivo.

Low-frequency stimulation at the troughs of theta-oscillation induces long-term depression of previously potentiated CA1 synapses

1996 ◽  
Vol 75 (2) ◽  
pp. 877-884 ◽  
Author(s):  
P. T. Huerta ◽  
J. E. Lisman
Keyword(s):  
Hippocampal Slices ◽  
Field Potential ◽  
Low Frequency ◽  
Long Term Depression ◽  
Low Frequency Stimulation ◽  
Bath Application ◽  
Stable Conditions ◽  
Theta Frequency ◽  
Frequency Stimulation

1. The induction of long-term weakening of synaptic transmission in rat hippocampal slices was examined in CA1 synapses during cholinergic modulation. 2. Bath application of the cholinergic agonist carbachol (50 microM) activated an oscillation of the local field potential in the theta-frequency range (5-12 Hz), termed theta. It was previously shown that a stimulation train of 40 single shocks (at 0.1 Hz) to the Schaffer collateral-commisural afferents, each synchronized with positive peaks of theta, caused homosynaptic long-term enhancement in CA1. Furthermore, long-term depression (LTD) was sporadically observed when the stimulation train was given at negative troughs of theta. Here we have sought to determine stable conditions for LTD induction during theta. 3. Synaptic weakening was reliably obtained, by giving 40 shocks (at 0.1 Hz) at theta-troughs, only in pathways that had been previously potentiated. This decrement, termed theta-LTD, was synapse specific because it did not occur in an independent pathway not stimulated during theta. The interval between the initial potentiating tetanus and theta-LTD induction could be as long as 90 min. 4. theta-LTD could be saturated; after consecutive episodes of theta-LTD induction, no significant further depression was obtained. Moreover, theta-LTD could be reversed by tetanic stimulation. 5. theta-LTD could prevent the induction of LTD by 600-900 pulses at 1 Hz. This suggests that the two protocols may share common mechanisms at the synaptic level. 6. We conclude that single presynaptic spikes that occur at low frequency and are properly timed to the troughs of theta may be a relevant mechanism for decreasing the strength of potentiated synapses.

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