Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons (original) (raw)
Related papers
2002
The interplay between principal cells and interneurons plays an important role in timing the activity of individual cells. We investigated the influence of single hippocampal CA1 pyramidal cells on putative interneurons. The activity of CA1 pyramidal cells was controlled intracellularly by current injection, and the activity of neighboring interneurons was recorded extracellularly in the urethane-anesthetized rat. Spike transmission probability between monosynaptically connected pyramidal cell-interneuron pairs was frequency dependent and highest between 5 and 25 Hz. In the awake animal, interneurons were found that had place-modulated firing rates, with place maps similar to their presynaptic pyramidal neuron. Thus, single pyramidal neurons can effectively determine the firing patterns of their interneuron targets.
The Journal of Physiology, 1998
1. Hippocampal non-principal neurons at the stratum radiatum-stratum lacunosummoleculare border (R-LM interneurons) of the CA1 area may constitute several cell classes and have been implicated in the generation of GABAergic unitary IPSPs. Using biocytinfilled electrodes we recorded R-LM interneurons intracellularly in vitro and determined their postsynaptic effects in concomitantly recorded pyramidal cells. 2. Light microscopic analysis revealed four populations of R-LM interneurons with distinct axons: (1) basket cells (n = 4) with axons predominantly ramifying in the pyramidal cell layer;
Trends in Neurosciences, 2004
The operation of neuronal networks crucially depends on a fast time course of signaling in inhibitory interneurons. Synapses that excite interneurons generate fast currents, owing to the expression of glutamate receptors of specific subunit composition. Interneurons generate brief action potentials in response to transient synaptic activation and discharge repetitively at very high frequencies during sustained stimulation. The ability to generate short-duration action potentials at high frequencies depends on the expression of specific voltage-gated K 1 channels. Factors facilitating fast action potential initiation following synaptic excitation include depolarized interneuron resting potential, subthreshold conductances and active dendrites. Finally, GABA release at interneuron output synapses is rapid and highly synchronized, leading to a faster inhibition in postsynaptic interneurons than in principal cells. Thus, the expression of distinct transmitter receptors and voltage-gated ion channels ensures that interneurons operate with high speed and temporal precision.
Interneurons, Spike Timing, and Perception
Neuron, 2001
glutamatergic excitation and the activity in specific brainstem cholinergic nuclei associated with the emer-2 Physiologie Cé ré brale CNRS FRE 2199 gence of ␥ oscillations in vivo. Interactions. Interneurons play a key role in the gene-Université Paris V 75006 Paris sis of ␥ oscillations (Bragin et al., 1995; Traub et al., 1999). While a persistent excitatory drive is needed, in-France hibitory cell interactions with other interneurons are crucial to sculpt the rhythm. These interactions are constrained by anatomical connectivity. The characteristic Rhythmic ␥ oscillations at 30-70 Hz in cortical and hippocampal slices depend on a maintained excitation axonal ramifications of two distinct types of inhibitory cells help us understand their involvement in the genera-and on interactions between interneurons and pyramidal cells. These interactions include gap-junctional tion of rhythmic oscillations. Most cortical and hippocampal inhibitory cells contact several hundreds of py-connections between inhibitory cells and fast excitatory and inhibitory chemical synapses. Spike timing ramidal cells, as well as several tens of inhibitory cells, so forming ideal cheerleaders for synchronous clapping. with precision in the range of several ms may be assured by biphasic signaling mechanisms operating at In fact, they act as inverse cheerleaders generating a periodic synaptic inhibition which dictates when pyrami-these different connections. Such temporal precision may be important in cognitive processing. dal cells do not fire. The second group of interneurons talk only to each other in a sort of cheerleaders cabal to propagate a coherent anti-clapping message. For Can clapping help us understand consciousness? Maybe it can. Studies in applause physics have exam-instance, a group of interneurons containing the calcium binding protein calretinin form inhibitory synapses ex-ined the delightful social self-organization that occurs when an audience claps at first randomly and then syn-clusively with other interneurons (Gulyas et al., 1996). Modeling work has shown how the superposition of chronously to express their pleasure after a performance (Neda et al., 2000). The mechanisms involved are remi-inhibitory synaptic events generated within such a network of spontaneously active inhibitory elements in-niscent of those for a synchronous inhibitory neuron activity which may underlie EEG rhythms associated duces synchrony (Traub et al., 1999). If inhibitory interactions within clusters of interneurons with activated cortical states. Cortical oscillations at ␥ frequencies of 30-70 Hz are associated with distinct suffice to generate autonomous rhythms, now it seems that excitatory interactions between the same cells act behaviors including perception, attention, and sensorimotor coordination. They have been suggested to link to sharpen up the synchrony. The excitation is mediated by gap junctions formed between interneurons. Gap neurons engaged in different aspects of a cognitive task. Recently, attention has focused on the possibility that junctions transmit electrical signals directly so that an action potential in one neuron induces, with minimal electrical coupling between inhibitory cells plays a crucial role in generating such synchronous activity. delay, a smaller spikelet in a coupled cell. This rapid communication underlies the involvement of gap junc-Both synchronized clapping and interneuron synchrony need several ingredients. First, an excitatory tions in many synchronous processes in the brain. The molecular basis for gap-junctional coupling con-drive-both the audience and the interneurons must be excited. Second, interactions-between neighbors in sists of the expression of proteins of the connexin family at coordinated membrane sites in connected cells. Con-the audience or between connected interneurons. Third, the population must be homogenous. If clappers persist nexin 36 (Cx36) is the major neuronal connexin. The in applauding at different rhythms or if interneuron propdeletion of this protein in two different knockout mice erties are too different, synchronous activity does not suggests that it contributes to ␥ frequency oscillations. emerge. We will consider each of these elements in turn. In both animals, gap-junctional coupling between in-The Ingredients of Interneuron-Based terneurons was largely absent. A 30-70 Hz synchrony Synchronies initiated by activating kainate or muscarinic receptors Excitatory Drive. Data on the role of ␥ oscillations in was maintained in hippocampal slices but at reduced perception originate in work on behaving animals. In
Interneuron and Pyramidal Cell Interplay During In Vitro Seizure-Like Events
Journal of Neurophysiology, 2006
Excitatory and inhibitory (EI) interactions shape network activity. However, little is known about the EI interactions in pathological conditions such as epilepsy. To investigate EI interactions during seizure-like events (SLE), we performed simultaneous dual and triple whole-cell and extracellular recordings in pyramidal cells and oriens interneurons in rat hippocampal CA1. We describe a novel pattern of interleaving EI activity during spontaneous in vitro SLEs generated by the potassium channel blocker 4aminopyridine in the presence of decreased magnesium. Interneuron activity was increased during interictal periods. During ictal discharges interneurons entered into long-lasting depolarization block (DB) with suppression of spike generation; simultaneously, pyramidal cells produced spike trains with increased frequency (6-14Hz) and correlation. Following this period of runaway excitation, interneuron post-ictal spiking resumed and pyramidal cells became progressively quiescent. We performed correlation measures of cell-pair interactions using either the spikes alone or the subthreshold postsynaptic interspike signals. EE spike correlation was notably increased during interneuron DB, while subthreshold EE correlation decreased. EI spike correlations increased at the end of SLEs, while II subthreshold correlations increased during DB. Our findings underscore the importance of complex cell-type specific neuronal interactions in the formation of seizure patterns.
Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving Rat
The Journal of neuroscience : the official journal of the Society for Neuroscience, 1999
We examined whether excitation and inhibition are balanced in hippocampal cortical networks. Extracellular field and single-unit activity were recorded by multiple tetrodes and multisite silicon probes to reveal the timing of the activity of hippocampal CA1 pyramidal cells and classes of interneurons during theta waves and sharp wave burst (SPW)-associated field ripples. The somatic and dendritic inhibition of pyramidal cells was deduced from the activity of interneurons in the pyramidal layer [int(p)] and in the alveus and st. oriens [int(a/o)], respectively. Int(p) and int(a/o) discharged an average of 60 and 20 degrees before the population discharge of pyramidal cells during the theta cycle, respectively. SPW ripples were associated with a 2.5-fold net increase of excitation. The discharge frequency of int(a/o) increased, decreased ("anti-SPW" cells), or did not change ("SPW-independent" cells) during SPW, suggesting that not all interneurons are innervated b...
The Journal of Physiology
1. Intracellular recordings were obtained from pyramidal, granule and hilar cells in transverse slices of guinea-pig hippocampus to examine synaptic interactions between GABAergic neurones. 2. In the presence of the convulsant compound 4-aminopyridine (4-AP), after fast excitatory amino acid (EAA) neurotransmission was blocked pharmacologically, large amplitude inhibitory postsynaptic potentials (IPSPs) occurred rhythmically (every 4-8 s) and synchronously in all principal cell populations (triphasic synchronized IPSPs). In the presence of the GABAA receptor blocker picrotoxin (PTX), a large amplitude IPSP continued to occur spontaneously in all principal cells simultaneously (monophasic synchronized IPSP). 3. Burst firing occurred simultaneously in a group of hilar neurones (synchronized bursting neurones) coincident with triphasic synchronized IPSPs in principal cells. After PTX was added, the bursts and the underlying depolarizing synaptic potentials were completely suppressed in some of the synchronized bursting neurones (type I hilar neurones), while others (type II hilar neurones) continued to fire in bursts coincident with monophasic synchronized IPSPs in principal cells. Intense hyperpolarization blocked burst firing and revealed underlying attenuated spikes of less than 10 mV, but did not uncover any underlying depolarizing synaptic potentials. 4. In type II hilar neurones, during sufficient hyperpolarization, spontaneous activity consisted of attenuated spikes. With depolarization, the small spikes began to trigger full size action potentials. These data suggest the presence of electrotonically remote spike initiation sites. 5. The morphology of synchronized bursting neurones was revealed by intracellular injection of the fluorescent dye Lucifer Yellow. Attempts to inject dye into one type II hilar neurone often resulted in the labelling of two to four cells (dye coupling). Dye coupling was not observed in type I hilar neurones. 6. These findings indicate that excitatory interactions synchronizing the firing of GABAergic neurones can occur in the absence of fast EAA neurotransmission. GABAergic neurones can become synchronized via their recurrent collaterals through the depolarizing action of synaptically activated GABAA receptors. In addition, a subpopulation of GABAergic neurones can become synchronized by a mechanism probably involving electrotonic coupling.
European Journal …, 1998
In the rat neocortex, a subset of GABAergic interneurons express the neuropeptide vasoactive intestinal peptide (VIP). Previously, we demonstrated that a population of VIPergic interneurons could be accurately identified by their irregular spiking (IS) pattern and their bipolar morphology. IS interneurons were studied in neocortical slices from 16-22-day-old rats using whole-cell recordings, intracellular labelling and single-cell RT-PCR. In response to a depolarizing pulse, IS interneurons typically discharged a burst of action potentials followed by spikes emitted at an irregular frequency. Several seconds of depolarization, micromolar concentrations of 4-aminopyridine, and nanomolar concentrations of either dendrotoxin I or K converted this irregular pattern to a sustained discharge, suggesting the involvement of an I D-like K ϩ current. The main glutamate receptor subunits detected in IS cells were GluR1 flop and GluR2 flop, GluR5 and GluR6, and NR2B and NR2D for the α-amino-3-hydroxyl-5-methyl-4-isoxazolepropionic acid (AMPA), kainate and N-methyl-D-aspartic acid (NMDA) subtypes, respectively. Paired whole-cell patch-clamp recordings indicated that pyramidal neurons provide intracortical glutamatergic inputs onto IS interneurons. Most connections had high probabilities of response and exhibited frequency-dependent paired pulse depression. Comparison of the amplitude distribution of paired responses suggested that most of these connections consisted of multiple functional release sites. Finally, two discrete subpopulations of IS cells could be identified based on the duration of the initial burst of action potentials and the differential expression of calretinin and choline acetyltransferase.