Unitary IPSPs evoked by interneurons at the stratum radiatum‐stratum lacunosum‐moleculare border in the CA1 area of the rat hippocampus in vitro

Abstract

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; (2) Schaffer collateralÏcommissural pathway-associated interneurons (n = 10) stratifying in stratum radiatum and, to a lesser extent, stratum oriens; (3) perforant pathway-associated interneurons (n = 6) innervating the perforant path termination zone in stratum lacunosum-moleculare of the CA1 area as well as equivalent portions of the dentate gyrus and subiculum; and (4) neurogliaform interneurons (n = 2) characterized by their dense, compact axonal and dendritic arbour. 3. Random electron microscopic sampling of synaptic targets revealed a preponderance of pyramidal neurons as postsynaptic elements. Basket cells had a synaptic target preference for somata and proximal dendrites, whereas the remainder of R-LM interneurons innervated dendritic shafts and spines. The axon of dendrite-targeting cells formed up to six putative contacts with individual postsynaptic pyramidal cells. 4. Anatomically recovered R-LM interneurons (n = 22) had a mean resting membrane potential of −56·7 ± 3·6 mV, a membrane time constant of 12·9 ± 7·7 ms and an input resistance of 86·4 ± 29·2 MÙ. Depolarizing current pulses generally elicited overshooting action potentials (70·8 ± 6·9 mV) which had a mean duration, when measured at halfamplitude, of 0·7 ± 0·1 ms. In response to prolonged ( > 200 ms) depolarizing current pulses all R-LM interneurons displayed (a varying degree of) spike frequency adaptation. 5. Basket cells, Schaffer-associated and neurogliaform interneurons elicited small-amplitude (< 2 mV), short-latency IPSPs in postsynaptic pyramids (n = 5, 13 and 1, respectively). Those interactions in which an effect was elicited with the repetitive activation of the presynaptic neuron (n = 13) showed a substantial degree of postsynaptic response summation. Unitary IPSPs had fast kinetics and, whenever tested (n = 5; 1 basket cell and 4 Schaffer-associated interneurons), were abolished by the GABAA receptor antagonist bicuculline. 6. Thus, R-LM interneurons comprise several distinct populations which evoke fast GABAA receptor-mediated IPSPs. The domain-specific innervation of postsynaptic pyramidal cells suggests functionally diverse effects on the integration of afferent information in functionally non-equivalent compartments of pyramidal cells.

What Determines the Frequency of Fast Network Oscillations With Irregular Neural Discharges? I. Synaptic Dynamics and Excitation-Inhibition Balance

“…The reversal potential of excitatory (inhibitory) synaptic currents is 0 mV (Ϫ70 mV). Synaptic conductances were calibrated such as the amplitude of PSCs was in the range of 0.2-2 mV at holding potential of Ϫ55 mV, i.e., just below threshold, in accordance with slice data Markram et al 1997;Tamas et al 1997Tamas et al , 1998Vida et al 1998). They yielded peak conductances, for AMPA receptors, ϳ1 nS; for NMDA receptors, ϳ0.01 nS; for GABA receptors, ϳ6 nS, compatible with experimentally inferred values (Bartos et al 2001(Bartos et al , 2002Gupta et al 2000;Markram et al 1997).…”

Networks of interneurons with fast and slow γ-aminobutyric acid type A (GABA A ) kinetics provide substrate for mixed gamma-theta rhythm

“…However, not all evidence supports the notion that these two populations are interconnected. For example, the small existing body of paired current-clamp recordings between presynaptic interneurons on the SR͞SL-M border and postsynaptic interneurons elsewhere does not show signs of slow synaptic connections (28,29). This discrepancy may be caused by the difficulty in distinguishing between fast and slow inputs under current clamp, or by the possibility that the presynaptic cells from the dual-cell recordings may not be the same ones activated by an extracellular stimulus in SL-M.…”

Interaction of nucleus reuniens and entorhinal cortex projections in hippocampal field CA1 of the rat

“…These interneurons are presumably Schaffer collaterals associated cholecystokinin-positive (CCK + ) cells which innervate pyramidal cells and other classes of interneurons, as well as each other (Nunzi et al 1985;Acsady et al 1996;Gulyás et al 1996;Vida et al 1998;Somogyi and Klausberger 2005 (Somogyi et al 1983;Li et al 1992;Kiss et al 1996. In addition, the presently described small sink-source pair at the pyramidal cell level in the RE/EC CSD (see Fig.…”