Facilitating pyramid to horizontal oriens‐alveus interneurone inputs: dual intracellular recordings in slices of rat hippocampus

Abstract

In adult rat hippocampal slices, simultaneous intracellular recordings from pyramidal cells in CA1 and interneurones near the stratum oriens‐alveus border revealed excitatory connections that displayed facilitation on repetitive activation in twelve of thirty‐six pairs tested. Postsynaptic interneurones were classified as horizontal oriens‐alveus interneurones by the pronounced ‘sag’ in response to hyperpolarizing current injection, high levels of spontaneous synaptic activity and by the morphology of their somata and dendrites, which were confined to stratum oriens‐alveus and their axons which projected to stratum lacunosum‐moleculare where they ramified extensively, in the region of entorhinal cortex input to CA1. Excitatory postsynaptic potentials (EPSPs) elicited by single pyramidal cells were 0 to 12 mV in amplitude. Mean EPSP amplitude (single spikes) was 0.93 ± 1.06 mV at −70 ± 2.3 mV (n= 10). The rise time was 1.2 ± 0.5 ms and the width at half‐amplitude was 7.5 ± 4.7 ms. EPSPs fluctuated greatly in amplitude; the mean coefficient of variation was 0.84 ± 0.37 for the first EPSP and 0.47 ± 0.24 for the second. Apparent failures of transmission frequently occurred after first presynaptic spikes but less frequently after the second or subsequent spikes in brief trains. EPSPs displayed facilitation at membrane potentials between −80 mV and spike threshold. Second EPSPs within 20 ms of the first were 253 ± 48% (range, 152–324%) of the mean first EPSP amplitude. Third EPSPs within 60 ms were 266 ± 70 % (range, 169–389%) and fourth EPSPs within 60–120 ms were 288 ± 71% (range, 188–393%). Both proportions of apparent failures of transmission and coefficient of variation analysis indicated a presynaptic locus for this facilitation.

Differential Expression of Group I Metabotropic Glutamate Receptors in Functionally Distinct Hippocampal Interneurons

“…The somatostatin-positive interneurons are interesting candidates for governing the time window in which oscillatory activity can take place. Because of the large convergence of many pyramidal cells onto somatostatin-positive interneurons (Ali and Thomson, 1998), these interneurons might sense the electrical activity of a large ensemble of pyramidal cells.…”

Nicotine Blocks the Hyperpolarization-Activated CurrentIhand Severely Impairs the Oscillatory Behavior of Oriens-Lacunosum Moleculare Interneurons

“…They have the soma and horizontal dendrites localized in stratum oriens and the axons targeting distal dendrites of CA1 pyramidal cells in stratum-lacunosum moleculare (Lacaille et al, 1987;Ali and Thomson, 1998;Maccaferri et al, 2000;Maccaferri, 2005). These neurons participate in hippocampal theta activity in vivo (Buzsáki, 2002;Klausberger et al, 2003) and in vitro (Pike et al, 2000;Gillies et al, 2002;Hájos et al, 2004;Gloveli et al, 2005).…”

“…We focused on somatostatin-expressing stratum oriens interneurons and in particular on O-LM cells, the predominant horizontal cell type in the CA1 hippocampal area (Ali and Thomson, 1998;Maccaferri, 2005), because these cells exhibit intrinsic resonance and spike transfer frequency preference in the theta range (Pike et al, 2000) and have been shown to contribute to the generation of the theta rhythm in vivo (Klausberger et al, 2003). To target this subpopulation, we used transgenic mice expressing enhanced green fluorescent protein (EGFP) in a subset of somatostatin-containing interneurons that mostly comprise O-LM cells in the CA1 stratum oriens (Oliva et al, 2000).…”

Quantal Size Is Independent of the Release Probability at Hippocampal Excitatory Synapses

“…It is widely accepted that short-term plasticity is accompanied by changes in P r (for review, see Thomson, 2000;Zucker and Regehr, 2002); however, whether alterations in P r (purely presynaptic) fully account for such plasticity (Gulyas et al, 1993;Paulsen and Heggelund, 1994;Stevens and Wang, 1995;Hanse and Gustafsson, 2001;Silver et al, 2003;Lawrence et al, 2004) or whether postsynaptic alterations also occur (Otis et al, 1996;Rozov and Burnashev, 1999;Oleskevich et al, 2000;Oertner et al, 2002;Harrison and Jahr, 2003) is still a question of active debate. To determine the quantal parameters and the locus of alterations during short-term facilitation at cortical glutamatergic synapses, we took advantage of the robust facilitation of synapses made by hippocampal CA1 pyramidal cells (PCs) onto specific subtypes of interneurons (Ali and Thomson, 1998;Scanziani et al, 1998;Losonczy et al, 2002). Because this facilitation is accompanied by a large change in P r (Ali and Thomson, 1998), we could study this connection under physiologically relevant but highly diverse P r conditions.…”

“…To determine the quantal parameters and the locus of alterations during short-term facilitation at cortical glutamatergic synapses, we took advantage of the robust facilitation of synapses made by hippocampal CA1 pyramidal cells (PCs) onto specific subtypes of interneurons (Ali and Thomson, 1998;Scanziani et al, 1998;Losonczy et al, 2002). Because this facilitation is accompanied by a large change in P r (Ali and Thomson, 1998), we could study this connection under physiologically relevant but highly diverse P r conditions. Our results demonstrate a sole presynaptic change during short-term facilitation and are consistent with the "one-release site, one-vesicle" hypothesis.…”