Gap Junction Modulation of Low-Frequency Oscillations in the Cerebellar Granule Cell Layer

Abstract

Local field potential (LFP) oscillations in the granule cell layer (GCL) of the cerebellar cortex have been identified previously in the awake rat and monkey during immobility. These low-frequency oscillations are thought to be generated through local circuit interactions between Golgi cells and granule cells within the GCL. Golgi cells display rhythmic firing and pacemaking properties, and also are electrically coupled through gap junctions within the GCL. Here, we tested if gap junctions in the rat cerebellar cortex contribute to the generation of LFP oscillations in the GCL. We recorded LFP oscillations under urethane anesthesia, and examined the effects of local infusion of gap junction blockers on 5-15 Hz oscillations. Local infusion of the gap junction blockers carbenoxolone and mefloquine resulted in significant decreases in the power of oscillations over a 30-min period, but the power of oscillations was unchanged in control experiments following vehicle injections. In addition, infusion of gap junction blockers had no significant effect on multi-unit activity, suggesting that the attenuation of low-frequency oscillations was likely due to reductions in electrical coupling rather than a decreased excitability within the granule cell layer. Our results indicate that electrical coupling among the Golgi cell networks in the cerebellar cortex contributes to the local circuit mechanisms that promote the occurrence of GCL LFP slow oscillations in the anesthetized rat.

Beta‐gamma burst stimulations of the inferior olive induce high‐frequency oscillations in the deep cerebellar nuclei

“…The ability to discharge at different rhythms allows them to carry additional information in a more efficient fashion than the average firing rate as it takes the exact spike timing into account (Jirenhed et al, 2017). The cerebellum displays various sorts of rhythmic activities covering both low-frequency (Courtemanche et al, 2002(Courtemanche et al, , 2013Courtemanche & Lamarre, 2005;D'Angelo et al, 2009;Dugu e et al, 2009;Robinson et al, 2017) and high-frequency oscillations (HFO) (Cheron et al, 2004(Cheron et al, , 2014Servais et al, 2005;de Solages et al, 2008).…”

Cerebellar Cortex 4–12 Hz Oscillations and Unit Phase Relation in the Awake Rat

“…LFP periods of strong oscillations, in contrast with periods when oscillations were weaker, were identified using spectrograms, calculated using the discrete short-time Fourier transform to evaluate rhythmicity. A multi-parametric algorithm was used to identify oscillatory periods in the 4–12 Hz band of the spectrogram, corresponding with rodent GCL oscillations from other in vivo studies (Hartmann and Bower, 1998 ; O’Connor et al, 2002 ; Dugué et al, 2009 ; Frederick et al, 2014 ; Robinson et al, 2017 ). This algorithm has been used previously to detect and process various rhythmic signals [gamma (Lévesque et al, 2009 ), and theta (Berryer et al, 2016 )].…”

“…Intrinsic oscillatory capacities of the GCL local network have been modeled (Maex and De Schutter, 2005 ; Dugué et al, 2009 ; Honda et al, 2011 ; Simões de Souza and De Schutter, 2011 ; Sudhakar et al, 2017 ). For instance, Golgi cell-mediated feedforward and feedback loops (Forti et al, 2006 ; D’Angelo, 2008 ; Dugué et al, 2009 ; Galliano et al, 2010 ), and Golgi-Golgi electrical synapses could be implicated in the rhythm formation (Dugué et al, 2009 ; Vervaeke et al, 2010 ; Simões de Souza and De Schutter, 2011 ; Robinson et al, 2017 ). Further in the circuit, in a limited dataset, we saw that Purkinje cell simple spikes (SSs) can follow the 10–25 Hz GCL rhythm, contrary to complex spikes (Courtemanche et al, 2002 ).…”

Norepinephrine controls the gain of the inhibitory circuit in the cerebellar input layer

“…Under these conditions, intrinsic activity and strong electrical coupling is expected to promote spike synchronization in the GoC network, as observed under anesthesia (van Welie et al, 2016). Previous work has shown that electrically-coupled GoC networks contribute to local field potential (LFP) oscillations in the theta band (~ 8 Hz) (Dugué et al, 2009;Robinson et al, 2017).…”