Abstract
Electrical synapses are ubiquitous in interneuron networks. They form intercellular pathways, allowing electrical currents to leak between coupled interneurons. I explored the impact of electrical coupling on the integration of excitatory signals and on the coincidence detection abilities of electrically-coupled cerebellar basket cells (BCs). In order to do so, I quantified the influence of electrical coupling on the rate, the probability and the latency at which BCs generate action potentials when stimulated. The long-lasting simultaneous suprathreshold depolarization of a coupled cell evoked an increase in firing rate and a shortening of action potential latency in a reference basket cell, compared to its depolarization alone. Likewise, the action potential probability of coupled cells was strongly increased when they were simultaneously stimulated with trains of short-duration near-threshold current pulses (mimicking the activation of presynaptic granule cells) at 10 Hz, and to a lesser extent at 50 Hz, an effect that was absent in non-coupled cells. Moreover, action potential probability was increased and action potential latency was shortened in response to synaptic stimulations in mice lacking the protein that forms gap junctions between BCs, connexin36, relative to wild-type (WT) controls. These results suggest that electrical synapses between BCs decrease the probability and increase the latency of stimulus-triggered action potentials, both effects being reverted upon simultaneous excitation of coupled cells. Interestingly, varying the delay at which coupled cells are stimulated revealed that the probability and the speed of action potential generation are facilitated maximally when a basket cell is stimulated shortly after a coupled cell. These findings suggest that electrically-coupled interneurons behave as coincidence and sequence detectors that dynamically regulate the latency and the strength of inhibition onto postsynaptic targets depending on the degree of input synchrony in the coupled interneuron network.
Highlights
Inhibitory interneurons control the timing of signals carried between and within brain areas by inhibiting action potential generation in principal neurons (Pouille and Scanziani, 2001; Brunel et al, 2004; Mittmann et al, 2005; Chu et al, 2012; Blot and Barbour, 2014)
In order to explore the modulation of basket cells (BCs) firing rate by electrical synapses (ESs) in response to coincident vs. non-coincident excitation, paired whole-cell recordings from electrically-coupled BCs were performed in acute slices from juvenile rats
Action potential firing responses of nearby electrically-coupled BCs were evoked by 500 ms duration depolarizing current pulses, first separated in time and simultaneously in both cells (Figure 1)
Summary
Inhibitory interneurons control the timing of signals carried between and within brain areas by inhibiting action potential generation in principal neurons (Pouille and Scanziani, 2001; Brunel et al, 2004; Mittmann et al, 2005; Chu et al, 2012; Blot and Barbour, 2014). Synaptic connections between interneurons play a critical role in coordinating the activity of interneuron networks, controlling the time windows during which action potentials can be generated by principal cells (Bartos et al, 2002). ESs have been proposed to equalize the membrane potential of electrically-coupled neurons, thereby synchronizing subthreshold and spiking activity and contributing to network oscillations (Mann-Metzer and Yarom, 1999; Deans et al, 2001; Galarreta and Hestrin, 2001a; Hormuzdi et al, 2001; Kopell and Ermentrout, 2004; van Welie et al, 2016). Computational models suggest that ESs may be effective in synchronizing neural networks only under certain conditions (Tchumatchenko and Clopath, 2014)
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