Presynaptic modulation of CA3 network activity

Staley, Kevin J.; Longacher, Mark; Bains, Jaideep S.; Yee, Audrey S.

doi:10.1038/651

Cited by 194 publications

(209 citation statements)

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“…Similar spontaneous bursts are also observed in epileptiform bursting in adult hippocampal CA3 networks (Staley et al 1998). Bouts of activity in these other systems are thought to be important for guiding the appropriate construction of the developing networks (Ben-Ari 2001;Katz and Shatz 1996;O'Donovan 1999).…”

Section: Bout Propertiesmentioning

confidence: 64%

Episodic Bouts of Activity Accompany Recovery of Rhythmic Output By a Neuromodulator- and Activity-Deprived Adult Neural Network

Luther

Robie

Yarotsky

et al. 2003

Journal of Neurophysiology

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. Episodic bouts of activity accompany recovery of rhythmic output by a neuromodulator-and activity-deprived adult neural network. J Neurophysiol 90: 2720 -2730, 2003. First published July 2, 2003 10.1152/jn.00370.2003. The pyloric rhythm of the stomatogastric ganglion of the crab, Cancer borealis, slows or stops when descending modulatory inputs are acutely removed. However, the rhythm spontaneously resumes after one or more days in the absence of neuromodulatory input. We recorded continuously for days to characterize quantitatively this recovery process. Activity bouts lasting 40 -900 s began several hours after removal of neuromodulatory input and were followed by stable rhythm recovery after 1-4 days. Bout duration was not related to the intervals (0.3-800 min) between bouts. During an individual bout, the frequency rapidly increased and then decreased more slowly. Photoablation of back-filled neuromodulatory terminals in the stomatogastric ganglion (STG) neuropil had no effect on activity bouts or recovery, suggesting that these processes are intrinsic to the STG neuronal network. After removal of neuromodulatory input, the phase relationships of the components of the triphasic pyloric rhythm were altered, and then over time the phase relationships moved toward their control values. Although at low pyloric rhythm frequency the phase relationships among pyloric network neurons depended on frequency, the changes in frequency during recovery did not completely account for the change in phase seen after rhythm recovery. We suggest that activity bouts represent underlying mechanisms controlling the restructuring of the pyloric network to allow resumption of an appropriate output after removal of neuromodulatory input.

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Section: Bout Propertiesmentioning

confidence: 64%

Episodic Bouts of Activity Accompany Recovery of Rhythmic Output By a Neuromodulator- and Activity-Deprived Adult Neural Network

Luther

Robie

Yarotsky

et al. 2003

Journal of Neurophysiology

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“…The concept of exhaustion of neurotransmitter release in the context of epileptiform bursting was first shown by Staley et al (1998) using an elevated extracellular K ϩ perfusate. CA3 pyramidal cell population burst duration was limited by depletion of the releasable glutamate pool at these recurrent synapses, even when the afterhyperpolarization, GABA A , and GABA B conductances were simultaneously blocked.…”

Section: Changes In the Balance Of Inhibition And Excitationmentioning

confidence: 99%

“…These results suggest that GABAmediated responses predominate during the early preictal phase, and the exhaustion of GABA release coincides with the ictus. Hence, one major factor determining the "balance" of excitation and inhibition during the transition into the high-frequency "ictal" state could be the relative ability of excitatory and inhibitory presynaptic terminals to release neurotransmitter, which will be affected by the ambient concentrations of extracellular potassium and calcium (Rausche et al, 1988;Seigneur and Timofeev, 2011), neurmodulatory effects of presynaptic receptors (GABA B and glutamate) (Peet and McLennan, 1986;Stafford et al, 2010), calcium buffering, and availability of vesicle pools (Rosenmund and Stevens, 1996;Staley et al, 1998).…”

Section: Changes In the Balance Of Inhibition And Excitationmentioning

confidence: 99%

Transition to Seizure: Ictal Discharge Is Preceded by Exhausted Presynaptic GABA Release in the Hippocampal CA3 Region

Zhang¹,

Koifman²,

Shin³

et al. 2012

J. Neurosci.

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How the brain transitions into a seizure is poorly understood. Recurrent seizure-like events (SLEs) in low-Mg 2ϩ /high-K ϩ perfusate were measured in the CA3 region of the intact mouse hippocampus. The SLE was divided into a "preictal phase," which abruptly turns into a higher frequency "ictal" phase. Blockade of GABA A receptors shortened the preictal phase, abolished interictal bursts, and attenuated the slow preictal depolarization, with no effect on the ictal duration, whereas SLEs were blocked by glutamate receptor blockade. In CA3 pyramidal cells and stratum oriens non-fast-spiking and fast-spiking interneurons, recurrent GABAergic IPSCs predominated interictally and during the early preictal phase, synchronous with extracellularly measured recurrent field potentials (FPs). These IPSCs then decreased to zero or reversed polarity by the onset of the higher-frequency ictus. However, postsynaptic muscimol-evoked GABA A responses remained intact. Simultaneously, EPSCs synchronous with the FPs markedly increased to a maximum at the ictal onset. The reversal potential of the compound postsynaptic currents (combined simultaneous EPSCs and IPSCs) became markedly depolarized during the preictal phase, whereas the muscimol-evoked GABA A reversal potential remained unchanged. During the late preictal phase, interneuronal excitability was high, but IPSCs, evoked by local stimulation, or osmotically by hypertonic sucrose application, were diminished, disappearing at the ictal onset. We conclude that the interictal and early preictal states are dominated by GABAergic activity, with the onset of the ictus heralded by exhaustion of presynaptic release of GABA, and unopposed increased glutamatergic responses.

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“…During partial bursts, the non-bursting cells of the network display low-frequency oscillations driven by synchronous subthreshold synaptic potentials . Three main variables have been shown to play an important role in modulating this type of network burst in the hippocampus: (1) the specific intrinsic properties of the participating neurons (Chamberlin and Dingledine, 1989;Kamondi et al, 1998;Fricker and Miles, 2001); (2) the strength of glutamatergic input originating from the recurrent collateral positive feedback of the CA3 region (Staley et al, 1998;Bains et al, 1999); and (3) the strength of GABAergic input (Korn et al, 1987;Staley et al, 1998).…”

Section: Introductionmentioning

confidence: 99%

Cell Type-Specific Synaptic Dynamics of Synchronized Bursting in the Juvenile CA3 Rat Hippocampus

Aradi

Maccaferri²

2004

J. Neurosci.

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Spontaneous synchronous bursting of the CA3 hippocampus in vitro is a widely studied model of physiological and pathological network synchronization. The role of inhibitory conductances during network bursting is not understood in detail, despite the fact that several antiepileptic drugs target GABA A receptors. Here, we show that the first manifestation of a burst event is a cell type-specific flurry of GABA A receptor-mediated inhibitory input to pyramidal cells, but not to stratum oriens horizontal interneurons. Moreover, GABA A receptor-mediated synaptic input is proportionally smaller in these interneurons compared with pyramidal cells. Computational models and dynamic-clamp studies using experimentally derived conductance waveforms indicate that both these factors modulate spike timing during synchronized activity. In particular, the different kinetics and the larger strength of GABAergic input to pyramidal cells defer action potential initiation and contribute to the observed delay of firing, so that the interneuronal activity leads the burst cycle. In contrast, excitatory inputs to both neuronal populations during a burst are kinetically similar, as required to maintain synchronicity. We also show that the natural pattern of activation of inhibitory and excitatory conductances during a synchronized burst cycle is different within the same neuronal population. In particular, GABA A receptor-mediated currents activate earlier and outlast the excitatory components driving the bursts. Thus, cell type-specific balance and timing of GABA A receptor-mediated input are critical to set the appropriate spike timing in pyramidal cells and interneurons and coordinate additional neurotransmitter release modulating burst strength and network frequency.

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Presynaptic modulation of CA3 network activity

Cited by 194 publications

References 50 publications

Episodic Bouts of Activity Accompany Recovery of Rhythmic Output By a Neuromodulator- and Activity-Deprived Adult Neural Network

Episodic Bouts of Activity Accompany Recovery of Rhythmic Output By a Neuromodulator- and Activity-Deprived Adult Neural Network

Transition to Seizure: Ictal Discharge Is Preceded by Exhausted Presynaptic GABA Release in the Hippocampal CA3 Region

Cell Type-Specific Synaptic Dynamics of Synchronized Bursting in the Juvenile CA3 Rat Hippocampus

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