scholarly journals Phasic Boosting of Medial Perforant Path-Evoked Granule Cell Output Time-Locked to Spontaneous Dentate EEG Spikes in Awake Rats

1998 ◽  
Vol 79 (6) ◽  
pp. 2825-2832 ◽  
Author(s):  
Clive R. Bramham
Keyword(s):  
Dentate Gyrus ◽  
Slow Wave ◽  
Granule Cell ◽  
Slow Wave Sleep ◽  
Population Spike ◽  
Perforant Path ◽  
Evoked Responses ◽  
Population Spike Amplitude ◽  
Output Time ◽  
Awake Rats

Bramham, Clive R. Phasic boosting of medial perforant path-evoked granule cell output time-locked to spontaneous dentate EEG spikes in awake rats. J. Neurophysiol. 79: 2825–2832, 1998. Dentate spikes (DSs) are positive-going field potential transients that occur intermittently in the hilar region of the dentate gyrus during alert wakefulness and slow-wave sleep. The function of dentate spikes is unknown; they have been suggested to be triggered by perforant path input and are associated with firing of hilar interneurons and inhibition of CA3 pyramidal cells. Here we investigated the effect of DSs on medial perforant path (MPP)-granule cell-evoked transmission in freely moving rats. The MPP was stimulated selectively in the angular bundle while evoked field potentials and the EEG were recorded with a vertical multielectrode array in the dentate gyrus. DSs were identified readily on the basis of their characteristic voltage-versus–depth profile, amplitude, duration, and state dependency. Using on-line detection of the DS peak, the timing of MPP stimulation relative to single DSs was controlled. DS-triggered evoked responses were compared with conventional, manually evoked responses in still-alert wakefulness (awake immobility) and, in some cases, slow-wave sleep. Input-output curves were obtained with stimulation on the positive DS peak (0 delay) and at delays of 50, 100, and 500 ms. Stimulation on the peak DS was associated with a significant increase in the population spike amplitude, a reduction in population spike latency, and a decrease in the field excitatory postsynaptic potential (fEPSP) slope, relative to manual stimulation. Granule cell excitability was enhanced markedly during DSs, as indicated by a mean 93% increase in the population spike amplitude and a leftward shift in the fEPSP-spike relation. Maximum effects occurred at the DS peak, and lasted between 50 and 100 ms. Paired-pulse inhibition of the population spike was unaffected, indicating intact recurrent inhibition during DSs. The results demonstrate enhancement of perforant path-evoked granule cell output time-locked to DSs. DSs therefore may function to intermittently boost excitatory transmission in the entorhinal cortex-dentate gyrus-CA3 circuit. Such a mechanism may be important in the natural induction of long-term potentiation in the dentate gyrus and CA3 regions.

Evoked Responses of the Dentate Gyrus During Seizures in Developing Gerbils With Inherited Epilepsy

2002 ◽  
Vol 88 (2) ◽  
pp. 783-793 ◽  
Author(s):  
Paul S. Buckmaster ◽  
Emilia H. Wong
Keyword(s):  
Dentate Gyrus ◽  
Granule Cell ◽  
Amplitude Ratio ◽  
Population Spike ◽  
Evoked Responses ◽  
Seizure Onset ◽  
Seizure Severity ◽  
Spike Amplitude ◽  
Population Spike Amplitude ◽  
Fepsp Slope

When they are 1–2 mo old, domesticated Mongolian gerbils begin having initially mild seizures which become more severe with age. To evaluate the development of this increasing seizure severity, we obtained field potential responses of the dentate gyrus to paired-pulse stimulation of the perforant path during seizures. In 18 gerbils that were 1.5–8.0 mo old, 73 seizures were analyzed. We measured population spike amplitude, the slope of the field excitatory postsynaptic potential (fEPSP), and the population spike amplitude ratio (2nd/1st) to evaluate excitatory and inhibitory synaptic processes. In gerbils <2 mo old, exposure to a novel environment was followed by an increase in population spike amplitude and then by seizure onset, but population spike amplitude ratio and fEPSP slope remained at baseline levels, and multiple population spikes were never evoked. As previously reported for chronically epileptic gerbils, these findings provide little evidence of a disinhibitory seizure-initiating mechanism in the dentate gyrus when young gerbils begin having seizures. In young gerbils evoked responses changed little during the behaviorally mild seizures. In contrast, most seizures in older gerbils included generalized convulsions, postictal depression, and evoked responses that changed dramatically. In older gerbils, shortly after seizure onset the dentate gyrus became hyperexcitable. Population spike amplitude and fEPSP slope peaked, and multiple population spikes were evoked, suggesting that mechanisms for seizure amplification and spread are more developed in older gerbils. Next, dentate gyrus excitability decreased precipitously, and population spike amplitude and fEPSP slope diminished. This period of hypoexcitability began before the end of the seizure, suggesting it may contribute to seizure termination. After the convulsive phase of the seizure, older gerbils remained motionless during a period of postictal depression, and population spike amplitude remained suppressed until the abrupt switch to normal exploratory activity. These findings suggest that the mechanisms of postictal depression may suppress granule cell excitability. The population spike amplitude ratio peaked after the convulsive phase and then gradually returned to the baseline level an average of 12 min after seizure onset, suggesting that granule cell inhibition recovers within minutes after a spontaneous seizure. Although it is unclear whether the seizure-related changes in evoked responses are a cause or an effect of increased seizure severity in older gerbils, their analysis provides clues about developmental changes in the mechanisms of seizure spread and termination.

Spontaneous Waves in the Dentate Gyrus of Slices From the Ventral Hippocampus

2004 ◽  
Vol 92 (6) ◽  
pp. 3385-3398 ◽  
Author(s):  
Laura Lee Colgin ◽  
Don Kubota ◽  
Fernando A. Brucher ◽  
Yousheng Jia ◽  
Erin Branyan ◽  
...  
Keyword(s):  
Gap Junctions ◽  
Dentate Gyrus ◽  
Granule Cell ◽  
Action Potentials ◽  
Slow Wave Sleep ◽  
Glutamate Release ◽  
Acetylcholinesterase Inhibitor ◽  
Granule Cell Layer ◽  
Perforant Path ◽  
The Waves

Spontaneous negative-going potentials occurring at an average frequency of 0.7 Hz were recorded from the dentate gyrus of slices prepared from the temporal hippocampus of young adult rats. These events (here termed “dentate waves”) in several respects resembled the dentate spikes described for freely moving rats during immobile behaviors and slow-wave sleep. Action potentials were observed on the descending portion of the in vitro waves and, as expected from this, whole cell recordings established that the waves were composed of depolarizing currents. Dentate waves appeared to be locally generated within the granule cell layer and were greatly reduced by antagonists of AMPA-type glutamate receptors or by lesions to the entorhinal cortex. Simultaneous recordings indicated that the waves were often synchronized in the inner and outer blades of the dentate gyrus. Knife cuts through the perforant path and the commissural/associational system did not eliminate synchronization, leaving electrotonic propagation via gap junctions as its probable cause. In accord with this, cuts that separated the two blades of the dentate eliminated synchronization between them, and a compound that inhibits gap junctions reduced wave activity. Dentate waves were regularly accompanied by sharp waves in field CA3 and were reduced in size by the acetylcholinesterase inhibitor, physostigmine. It is hypothesized that dentate waves occur when spontaneous glutamate release from dentate afferents produces action potentials in neighboring granule cells that then summate electrotonically into a population event; once initiated, the waves propagate, again electrotonically, and thereby engage a significant portion of the granule cell population.

Nonlinear systems analysis of the hippocampal perforant path-dentate projection. II. Effects of random impulse train stimulation

1988 ◽  
Vol 60 (3) ◽  
pp. 1077-1094 ◽  
Author(s):  
T. W. Berger ◽  
J. L. Eriksson ◽  
D. A. Ciarolla ◽  
R. J. Sclabassi
Keyword(s):  
Nonlinear Systems ◽  
Granule Cell ◽  
Hippocampal Formation ◽  
Population Spike ◽  
Perforant Path ◽  
Dentate Granule Cell ◽  
Spike Amplitude ◽  
Population Spikes ◽  
Population Spike Amplitude ◽  
Interstimulus Intervals

1. Nonlinear systems analytic techniques were used to characterize transformational properties of the network of neurons activated by perforant path input to the rabbit hippocampus. Trains of 4,064 impulses with randomly varying interimpulse intervals were used to stimulate perforant path fibers, and amplitudes of evoked dentate granule cell population spikes were measured. Interimpulse intervals of the random stimulus train were determined by a Poisson distribution with a mean interimpulse interval of 500 ms, and with intervals ranging from 1 to 5,000 ms. The response of dentate granule cells to this stimulation was assumed to reflect activity in the larger hippocampal network, because other subpopulations of neurons activated monosynaptically and polysynaptically within the hippocampal formation contribute to granule cell excitability through multiple feedforward and feedback pathways. System properties were characterized both for halothane anesthetized and chronically implanted, unanesthetized preparations. 2. Second-order kernel analysis showed that population spike amplitude was highly dependent on interimpulse interval. When population spikes of all latencies were included in the same analysis, stimulation impulses produced near-total suppression of spike amplitude when they were preceded 10-20 ms by another impulse in the train. Spike suppression extended to approximately 50 ms and was inversely related to length of the interimpulse interval. Suppression of granule cell response to intervals within the range of 10-50 ms was not influenced by halothane anesthesia. 3. Interstimulus intervals greater than approximately 50 ms resulted in a facilitation of population spike amplitude, with maximum facilitation occurring in response to intervals of 90-100 ms. The magnitude of maximum facilitation was significantly greater for anesthetized (129%) than for unanesthetized (74%) preparations. The range of intervals resulting in facilitation for unanesthetized animals could extend to 1,000-1,100 ms (average range, 61-714 ms). This was much greater than observed for population spikes recorded from anesthetized animals (50-364 ms), which exhibited suppression in response to intervals of approximately 300-700 ms. 4. Further analysis revealed that the nature of nonlinearities in population spike amplitude may depend on spike latency. For example, population spikes of "short" latency (3-4 or 4-5 ms, depending on the animal) exhibited only facilitation in response to interstimulus intervals of 1-4 ms.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals NMDA Receptor-Dependent Plasticity of Granule Cell Spiking in the Dentate Gyrus of Normal and Epileptic Rats

2000 ◽  
Vol 84 (6) ◽  
pp. 2868-2879 ◽  
Author(s):  
M. Lynch ◽  
Ü. Sayin ◽  
G. Golarai ◽  
T. Sutula
Keyword(s):  
Nmda Receptor ◽  
Dentate Gyrus ◽  
Granule Cell ◽  
Granule Cells ◽  
Perforant Path ◽  
Spike Generation ◽  
Bathing Medium ◽  
Burst Discharge ◽  
Dependent Component ◽  
Single Spike

Because granule cells in the dentate gyrus provide a major synaptic input to pyramidal neurons in the CA3 region of the hippocampus, spike generation by granule cells is likely to have a significant role in hippocampal information processing. Granule cells normally fire in a single-spike mode even when inhibition is blocked and provide single-spike output to CA3 when afferent activity converging into the entorhinal cortex from neocortex, brainstem, and other limbic regions increases. The effects of enhancement of N-methyl-d-aspartate (NMDA) receptor-dependent excitatory synaptic transmission and reduction in γ-aminobutyric acid-A (GABAA) receptor-dependent inhibition on spike generation were examined in granule cells of the dentate gyrus. In contrast to the single-spike mode observed in normal bathing conditions, perforant path stimulation in Mg2+-free bathing conditions evoked graded burst discharges in granule cells which increased in duration, amplitude, and number of spikes as a function of stimulus intensity. After burst discharges were evoked during transient exposure to bathing conditions that relieve the Mg2+ block of the NMDA receptor, there was a marked increase in the NMDA receptor-dependent component of the EPSP, but no significant increase in the non-NMDA receptor-dependent component of the EPSP in normal bathing medium. Supramaximal perforant path stimulation still evoked only a single spike, but granule cell spike generation was immediately converted from a single-spike firing mode to a graded burst discharge mode when inhibition was then reduced. The induction of graded burst discharges in Mg2+-free conditions and the expression of burst discharges evoked in normal bathing medium with subsequent disinhibition were both blocked bydl-2-amino-4-phosphonovaleric acid (APV) and were therefore NMDA receptor dependent, in contrast to long-term potentiation (LTP) in the perforant path, which is induced by NMDA receptors and is also expressed by α-amino-3-hydroxy-5-methyl-4-isoxazoleproprionate (AMPA) receptors. The graded burst discharge mode was also observed in granule cells when inhibition was reduced after a single epileptic afterdischarge, which enhances the NMDA receptor-dependent component of evoked synaptic response, and in the dentate gyrus reorganized by mossy fiber sprouting in kindled and kainic acid-treated rats. NMDA receptor-dependent plasticity of granule cell spike generation, which can be distinguished from LTP and induces long-term susceptibility to epileptic burst discharge under conditions of reduced inhibition, could modify information processing in the hippocampus and promote epileptic synchronization by increasing excitatory input into CA3.

scholarly journals Acute Intrahippocampal Infusion of BDNF Induces Lasting Potentiation of Synaptic Transmission in the Rat Dentate Gyrus

1998 ◽  
Vol 79 (1) ◽  
pp. 496-499 ◽  
Author(s):  
Elhoucine Messaoudi ◽  
Kjetil Bårdsen ◽  
Bolek Srebro ◽  
Clive R. Bramham
Keyword(s):  
Synaptic Transmission ◽  
Dentate Gyrus ◽  
Granule Cells ◽  
Molecular Layer ◽  
Epileptiform Activity ◽  
Population Spike ◽  
Perforant Path ◽  
Excitatory Postsynaptic Potential ◽  
Adult Rats ◽  
Fepsp Slope

Messaoudi, Elhoucine, Kjetil Bårdsen, Bolek Srebro, and Clive R. Bramham. Acute intrahippocampal infusion of BDNF induces lasting potentiation of synaptic transmission in the rat dentategyrus. J. Neurophysiol. 79: 496–499, 1998. The effect of acuteintrahippocampal infusion of brain-derived neurotrophic factor (BDNF) on synaptic transmission in the dentate gyrus was investigated in urethan-anesthetized rats. Medial perforant path-evoked field potentials were recorded in the dentate hilus and BDNF-containing buffer was infused (4 μl, 25 min) immediately above the dentate molecular layer. BDNF led to a slowly developing increase of the field excitatory postsynaptic potential (fEPSP) slope and population spike amplitude. The potentiation either reached a plateau level at ∼2 h after BDNF infusion or continued to increase for the duration of experiment; the longest time point recorded was 10 h. Mean increases at 4 h after BDNF infusion were 62.2 and 224% for the fEPSP slope and population spike, respectively. No changes in responses were observed in controls receiving buffer medium only or buffer containing cytochrome C. BDNF-induced potentiation developed in the absence of epileptiform activity in the hippocampal electroencephalogram or changes in recurrent inhibition on granule cells as assessed by paired-pulse inhibition of the population spike. We conclude that exogenous BDNF induces a lasting potentiation of synaptic efficacy in the dentate gyrus of anesthetized adult rats.

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