Local circuit synaptic interactions in hippocampal brain slices

Knowles, W. Douglas; Schwartzkroin, Philip A.

doi:10.1523/jneurosci.01-03-00318.1981

Cited by 296 publications

(129 citation statements)

References 21 publications

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“…Firstly, local neuronal circuitry can be studied more directly than was previously possible (MacVicar andDudek 1980, Knowles andSchwartzkroin 1981) by the combination of electrophysiology, staining of neurones with fluorescent dyes and image analysis. Pairs of neurones can be filled with fluorescent dyes during simultaneous whole-cell recording.…”

Section: Discussionmentioning

confidence: 99%

A thin slice preparation for patch clamp recordings from neurones of the mammalian central nervous system

et al. 1989

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Abstract.(1) A preparation is described which allows patch clamp recordings to be made on mammalian central nervous system (CNS) neurones in situ. (2) A vibrating tissue slicer was used to cut thin slices in which individual neurones could be identified visually. Localized cleaning of cell somata with physiological saline freed the cell membrane, allowing the formation of a high resistance seal between the membrane and the patch pipette. (3) The various configurations of the patch clamp technique were used to demonstrate recording of membrane potential, whole cell currents and single channel currents from neurones and isolated patches. (4) The patch clamp technique was used to record from neurones filled with fluorescent dyes. Staining was achieved by filling cells during recording or by previous retrograde labelling. (5) Thin slice cleaning and patch clamp techniques were shown to be applicable to the spinal cord and almost any brain region and to various species. These techniques are also applicable to animals of a wide variety of postnatal ages, from newborn to adult.

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Section: Discussionmentioning

confidence: 99%

A thin slice preparation for patch clamp recordings from neurones of the mammalian central nervous system

et al. 1989

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“…Depending on how a slice is cut, the 500-600 ìm intergroup separation may be either about right, or too small, for the CA1 pyramidal cell axon spread. On the other hand, CA1 pyramidal cell collaterals are expected to innervate cells in target fields with lower probability than do basket cells (Knowles & Schwartzkroin, 1981;Sik et al 1995), so that the effect of longer-range CA1 pyramidal axons may not be critical. Of course, basket cells and pyramidal cells do not exist in a 1:1 ratio in the hippocampus, interneurones of all types constituting a minority of the cells.…”

Section: Simulation Methodsmentioning

confidence: 99%

“…With tetanic stimulation at two or more sites, oscillations in CA1 can become tightly synchronized (< 1 ms mean phase lag) at distances of at least 4·5 mm (Traub, Whittington, Stanford & Jefferys, 1996b; I. M. Stanford & J. G. R. Jefferys, unpublished data), so that an important feature of the in vivo phenomenon is captured in vitro. The relative sparseness of pyramidal cell-pyramidal cell synaptic connections in CA1 in vitro (Knowles & Schwartzkroin, 1981;Christian & Dudek, 1988;Thomson & Radpour, 1991) renders the analysis of the circuitry simpler than is the case in the neocortex. Electrophysiological data from the CA1 region in vitro, along with network simulations of compartmental neurones, suggest that synaptically interconnected networks of interneurones alone can generate ã oscillations, but that the properties of the oscillation are modified, in important ways, by the participation of pyramidal cells.…”

mentioning

confidence: 99%

Spatiotemporal patterns of γ frequency oscillations tetanically induced in the rat hippocampal slice

Whittington

Stanford

Colling

et al. 1997

The Journal of Physiology

209

204

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We used transverse and longitudinal rat hippocampal slices to study the synchronization of γ frequency (> 20 Hz) oscillations, across distances of up to 4.5 mm. γ oscillations were evoked in the CA1 region by tetanic stimulation at one or two sites simultaneously, and were associated with population spikes. Tetanic stimuli that were strong enough to induce oscillations were associated with depolarization of both pyramidal cells and interneurones, largely produced by activation of metabotropic glutamate receptors. Computer simulations of γ oscillations were also performed in a model with pyramidal cells and interneurones, arranged in a chain of five cell groups. This model had suggested previously that interneurone networks alone could generate synchronous γ oscillations locally, but that pyramidal cell firing, by inducing spike doublets in interneurones, was necessary for the occurrence of highly correlated oscillations with small phase lag (< 2.5 ms), in a distributed network possessing long axon conduction delays. In both experiment and model, pyramidal cell spikes occurred in phase with local population spikes, as did the first spike of the interneurone doublet. The conductance of the interneurone α‐amino‐3‐hydroxy‐5‐methyl‐4‐isoxazole propionic acid (AMPA) receptor‐mediated conductance was manipulated in the model, while the relation between oscillations at opposite ends of the chain was examined. When the conductance was large enough for doublet firing to be synaptically induced in interneurones, oscillation phase lags were < 2.25 ms across the chain. As predicted, experimental blockade of AMPA receptors resulted in increased phase lags between two sites oscillating simultaneously, compared with control conditions. Both in model and in experiment, when stimuli to the two ends of the network were slightly different, cross‐network synchronization occurred with a shorter phase lag at high frequencies than at lower frequencies. These data suggest that, while interneurone networks alone can generate locally synchronized γ oscillations, firing of pyramidal cells, and the synaptically induced doublet firing in interneurones, contribute to the stability and tight synchrony of the oscillations in distributed networks.

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“…The first studies of morphologically identified interneurons reported that interneurons were characterized by brief-duration action potentials, and therefore have been referred to as "fast-spiking" cells (Schwartzkroin and Mathers, 1978;Knowles and Schwartzkroin, 1981;McCormick et al, 1985). In addition, interneurons are characterized by a large afterhyperpolarization following action potentials, weak spike frequency adaptation, and short time constants (Schwartzkroin and Mathers, 1978;McCormick et al, 1985;Lacaille et al, 1987;Lacaille and Schwartzkroin, 1988;Lacaille and Williams, 1990;Scharfman, 1992b).…”

Section: Intrinsic Properties and Patterns Of Dischargementioning

confidence: 99%

“…Pyramidal-shaped cells were also distinct in that they often adapted. Many hippocampal interneurons do not appear to adapt (Schwartzkroin and Mathers, 1978;Knowles and Schwartzkroin, 1981) although there arc exceptions (Kawaguchi and Hama, 1990;Lacaille and Williams, 1990;Buhl et al, 1994b;Han, 1994). It is difficult to make a rigorous comparison of adaptation among different types of interneurons because previous studies have not necessarily quantified adaptation nor have they examined it in similar ways.…”

Section: Intrinsic Properties and Patterns Of Dischargementioning

confidence: 99%

Electrophysiological diversity of pyramidal‐shaped neurons at the granule cell layer/hilus border of the rat dentate gyrus recorded in vitro

Scharfman

1995

Hippocampus

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In the rat dentate gyrus, pyramidal-shaped cells located on the border of the granule cell layer and the hilus are one of the most common types of γ-aminobutyric acid (GABA)-immunoreactive neurons. This study describes their electrophysiological characteristics. Membrane properties, patterns of discharge, and synaptic responses were recorded intracellularly from these cells in hippocampal slices. Each cell was identified as pyramidal-shaped by injecting the marker Neurobiotin intracellularly (n = 17).In several respects the membrane properties of the sampled cells were similar to "fast-spiking" cells (putative inhibitory interneurons) that have been described in other areas of the hippocampus. For example, input resistance was high (mean 91.3 megohms), the membrane time constant was short (mean 7.7 ms), and there was a large afterhyperpolarization following a single action potential (mean 10.5 mV at resting potential). However, the action potentials of most pyramidalshaped cells were not as brief (mean 1.2 ms total duration) as those of most previously described fast-spiking cells. Many pyramidal-shaped neurons had strong spike frequency adaptation relative to other fast-spiking cells. Although these latter two characteristics were apparent in the majority of the sampled cells, there were exceptional pyramidal-shaped neurons with fast action potentials and weak adaptation, demonstrating the electrophysiological variability of pyramidal-shaped cells.Responses to outer molecular layer stimulation were composed primarily of excitatory postsynaptic potentials (EPSPs) rather than inhibitory postsynaptic potentials (IPSPs), and were usually small (EPSPs evoked at threshold were often less than 2 mV), and brief (less than 30 ms). There was variability, because in a few cells EPSPs evoked at threshold were much larger. However, regardless of EPSP amplitude, suprathreshold stimulation (up to 4 times the threshold stimulus strength) rarely evoked more than one action potential in any cell. The results suggest that stimulation of perforant path axons produces limited excitatory synaptic responses in pyramidal-shaped neurons. This may be one of the reasons why they are relatively resistant to prolonged perforant path stimulation.The pyramidal-shaped neurons located at the base of the granule cell layer have been associated historically with a basket plexus around granule cell somata, and have been called pyramidal "basket" cells. However, basket-like endings were rare and axon collaterals outside the granule cell layer were common. Many axon collaterals were as far from the granule cell layer as the outer molecular layer and the central hilus, and antidromic action potentials could be recorded in some

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Local circuit synaptic interactions in hippocampal brain slices

Cited by 296 publications

References 21 publications

A thin slice preparation for patch clamp recordings from neurones of the mammalian central nervous system

A thin slice preparation for patch clamp recordings from neurones of the mammalian central nervous system

Spatiotemporal patterns of γ frequency oscillations tetanically induced in the rat hippocampal slice

Electrophysiological diversity of pyramidal‐shaped neurons at the granule cell layer/hilus border of the rat dentate gyrus recorded in vitro

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