Abstract
The inferior olive (IO) forms one of the major gateways for information that travels to the cerebellar cortex. Olivary neurons process sensory and motor signals that are subsequently relayed to Purkinje cells. The intrinsic subthreshold membrane potential oscillations of the olivary neurons are thought to be important for gating this flow of information. In vitro studies have revealed that the phase of the subthreshold oscillation determines the size of the olivary burst and may gate the information flow or encode the temporal state of the olivary network. Here, we investigated whether the same phenomenon occurred in murine olivary cells in an intact olivocerebellar system using the in vivo whole-cell recording technique. Our in vivo findings revealed that the number of wavelets within the olivary burst did not encode the timing of the spike relative to the phase of the oscillation but was related to the amplitude of the oscillation. Manipulating the oscillation amplitude by applying Harmaline confirmed the inverse relationship between the amplitude of oscillation and the number of wavelets within the olivary burst. Furthermore, we demonstrated that electrotonic coupling between olivary neurons affect this modulation of the olivary burst size. Based on these results, we suggest that the olivary burst size might reflect the “expectancy” of a spike to occur rather than the spike timing, and that this process requires the presence of gap junction coupling.
Highlights
The inferior olive (IO) forms the sole source of climbing fiber inputs to Purkinje cells in the cerebellar cortex (Szentágothai and Rajkovits, 1959; Desclin, 1974)
Olivary neurons that were recorded under ketamine and xylazine (KX) and MMF conditions revealed similar basic membrane properties (Table 1), and these properties were comparable to those obtained in previous ex vivo measurements (Llinás and Yarom, 1981; Long et al, 2002; De Zeeuw et al, 2003; Leznik and Llinas, 2005)
To find out whether the phase of the subthreshold oscillations determines the number of wavelets in an olivary spike in vivo, we counted the number of wavelets that were superimposed on the spike ADP (Figure 1B; see arrows) and examined their dependency on the phase and amplitude of the subthreshold oscillation
Summary
The inferior olive (IO) forms the sole source of climbing fiber inputs to Purkinje cells in the cerebellar cortex (Szentágothai and Rajkovits, 1959; Desclin, 1974). Climbing fibers may fire in bursts (Crill and Kennedy, 1967; Crill, 1970; Maruta et al, 2007; Mathy et al, 2009) and thereby they can modify the complex spike (Mathy et al, 2009) These climbing fiber bursts are generated at the axon hillock of olivary cells and they backpropagate to the soma where they give rise to small wavelets (Mathy et al, 2009). The subthreshold oscillations may serve as a timekeeping device, whereas the gap junctions (i.e., connexin 36) may be necessary to form functional ensembles of Abbreviations: IO, inferior olive; Cx36, connexin 36; C57BL/6 mice, C57 black 6 mice; WT, wild type; KX, ketamine and xylazine; MMF, medetomidine, midazolam, and fentanyl; SSTO, sinusoidal subthreshold oscillation; LTO, low-threshold calcium (Ca2+) oscillation; ADP, afterdepolarization; SEM, standard error of the mean
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