Through a combination of intrinsic and synaptic properties, synchronous activation of a small number of Purkinje cells can set the spike timing of target neurons in the cerebellar nuclei. The sole output of the cerebellar cortex consists of Purkinje cells, which are GABAergic, and hence expected to inhibit their targets, the cerebellar nuclei. However, an inverse relationship in firing rate is not always observed between Purkinje and nuclear cells. Abigail Person and Indira Raman now propose that through a combination of kinetics, intrinsic firing rates and convergence of projections, synchronous activation of a small number of Purkinje cells can transmit information about spike timing. This work suggests a role for synchronous activity previously reported in cerebellar cortex, and demonstrates more generally how synchronous inhibition could be used to generate phase-locked activity. An unusual feature of the cerebellar cortex is that its output neurons, Purkinje cells, release GABA (γ-aminobutyric acid). Their high intrinsic firing rates1 (50 Hz) and extensive convergence2,3 predict that their target neurons in the cerebellar nuclei would be largely inhibited unless Purkinje cells pause their spiking, yet Purkinje and nuclear neuron firing rates do not always vary inversely4. One indication of how these synapses transmit information is that populations of Purkinje neurons synchronize their spikes during cerebellar behaviours5,6,7,8,9,10,11. If nuclear neurons respond to Purkinje synchrony, they may encode signals from subsets of inhibitory inputs7,12,13,14. Here we show in weanling and adult mice that nuclear neurons transmit the timing of synchronous Purkinje afferent spikes, owing to modest Purkinje-to-nuclear convergence ratios (∼40:1), fast inhibitory postsynaptic current kinetics (τdecay = 2.5 ms) and high intrinsic firing rates (∼90 Hz). In vitro, dynamically clamped asynchronous inhibitory postsynaptic potentials mimicking Purkinje afferents suppress nuclear cell spiking, whereas synchronous inhibitory postsynaptic potentials entrain nuclear cell spiking. With partial synchrony, nuclear neurons time-lock their spikes to the synchronous subpopulation of inputs, even when only 2 out of 40 afferents synchronize. In vivo, nuclear neurons reliably phase-lock to regular trains of molecular layer stimulation. Thus, cerebellar nuclear neurons can preferentially relay the spike timing of synchronized Purkinje cells to downstream premotor areas.

Purkinje neuron synchrony elicits time-locked spiking in the cerebellar nuclei