Abstract
Electrical coupling between some subclasses of interneurons is thought to promote coordinated firing that generates rhythmic synchronous activity in cortical regions. Synaptic activity of cholecystokinin (CCK) interneurons which co-express cannabinoid type-1 (CB1) receptors are powerful modulators of network activity via the actions of endocannabinoids. We investigated the modulatory actions of endocannabinoids between chemically and electrically connected synapses of CCK cells using paired whole-cell recordings combined with biocytin and double immunofluorescence labeling in acute slices of rat hippocampus at P18–20 days. CA1 stratum radiatum CCK Schaffer collateral-associated cells were coupled electrically with each other as well as CCK basket cells and CCK cells with axonal projections expanding to dentate gyrus. Approximately 50% of electrically coupled cells received facilitating, asynchronously released inhibitory postsynaptic potential (IPSPs) that curtailed the steady-state coupling coefficient by 57%. Tonic CB1 receptor activity which reduces inhibition enhanced electrical coupling between cells that were connected via chemical and electrical synapses. Blocking CB1 receptors with antagonist, AM-251 (5 μM) resulted in the synchronized release of larger IPSPs and this enhanced inhibition further reduced the steady-state coupling coefficient by 85%. Depolarization induced suppression of inhibition (DSI), maintained the asynchronicity of IPSP latency, but reduced IPSP amplitudes by 95% and enhanced the steady-state coupling coefficient by 104% and IPSP duration by 200%. However, DSI did not did not enhance electrical coupling at purely electrical synapses. These data suggest that different morphological subclasses of CCK interneurons are interconnected via gap junctions. The synergy between the chemical and electrical coupling between CCK cells probably plays a role in activity-dependent endocannabinoid modulation of rhythmic synchronization.
Highlights
Network oscillations are thought to be generated by combined synchronous entrainment of inhibitory postsynaptic potentials (IPSP) onto pyramidal cells
MORPHOLOGICAL AND MEMBRANE PROPERTIES OF CCK INTERNEURONS Cholecystokinin-positive Schaffer collateral-associated (SCA) cell bodies were found in stratum radiatum (SR) and stratum lacunosum moleculare (SLM)
Our results demonstrate that electrical coupling between CCK interneurons of the CA1 region occur between cells of the same morphological subclass and connections between heterogeneous cell types
Summary
Network oscillations are thought to be generated by combined synchronous entrainment of inhibitory postsynaptic potentials (IPSP) onto pyramidal cells. Recent studies have demonstrated that several other non-fast spiking subclasses of interneurons in the neocortex are interconnected via electrical synapses, including neocortical irregular-spiking interneurons that express cannabinoid type-1 (CB1) receptors (Galarreta et al, 2004, 2008 see Gibson et al, 1999) and calretinin interneurons (Caputi et al, 2009) The exception to this rule seems to be the neuroglia form (NGF) cell, as they are coupled electrically with each other as well as to other interneuron subclasses in the neocortex (Simon et al, 2005). CCK cells that are connected chemically have the ability to allow more temporal and spatial flexibility as they can switch between synchronous and asynchronous release of GABA via CB1 receptors (Ali and Todorova, 2010) Whether these modulatory actions extend to modulating electrically coupled CCK synapses that are paired with chemical synapses was investigated using dual whole-cell recordings combined with biocytin and double immunofluorescence labeling in acute slices of P18–20 day old rat hippocampus
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