Inhibitory control of intracerebellar nuclei by the Purkinje cell axons

Ito, Masao; Yoshida, Masaki; Obata, Kunihiko; Kawai, Nobufumi; Udo, M.

doi:10.1007/bf00340519

Cited by 269 publications

(92 citation statements)

References 34 publications

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“…Because Purkinje cells are tonically active and inhibitory onto CN neurons (Ito and Yoshida, 1966;Ito et al, 1970) and because CN neurons are themselves autonomous pacemakers (Thach, 1968;Raman et al, 2000), it is often assumed that cerebellar nuclear neurons simply invert signals from Purkinje cells. Data collected in both behaving monkeys and decerebrate cats have been equivocal in supporting these assumptions, however.…”

Section: Synchrony Of Purkinje Cells Can Elicit Time-locked Spiking Imentioning

confidence: 99%

The Neuronal Code(s) of the Cerebellum

et al. 2013

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Understanding how neurons encode information in sequences of action potentials is of fundamental importance to neuroscience. The cerebellum is widely recognized for its involvement in the coordination of movements, which requires muscle activation patterns to be controlled with millisecond precision. Understanding how cerebellar neurons accomplish such high temporal precision is critical to understanding cerebellar function. Inhibitory Purkinje cells, the only output neurons of the cerebellar cortex, and their postsynaptic target neurons in the cerebellar nuclei, fire action potentials at high, sustained frequencies, suggesting spike rate modulation as a possible code. Yet, millisecond precise spatiotemporal spike activity patterns in Purkinje cells and inferior olivary neurons have also been observed. These results and ongoing studies suggest that the neuronal code used by cerebellar neurons may span a wide time scale from millisecond precision to slow rate modulations, likely depending on the behavioral context. IntroductionThe cerebellum has long been regarded as a purely sensorimotorrelated structure, crucial for the precise temporal coordination of body, limb, and eye movements and the learning and fine-tuning of motor skills. Electrophysiological investigations of the cerebellar cortical principal neurons, the Purkinje cells, and their postsynaptic targets, the neurons in the cerebellar nuclei (CN) and vestibular nuclei, revealed strong representations of a wide variety of sensory and motor events (Ito, 1984; Strata, 1989) in the presence of high sustained spike rates (Thach, 1972).Extracellular single-unit recordings, particularly those conducted in awake and behaving nonhuman primates, have established that Purkinje cell simple spike rates represent a variety of variables related to the control of eye, head, and limb movements. Encoded variables include the direction of limb movements (e.g., Harvey et al., 1977; Thach, 1978; Fortier et al., 1989; Smith et al., 1993) and limb movement velocity or speed (Coltz et al., 1999; Roitman et al., 2005). Studies of arm movement dynamics provided evidence that Purkinje cell simple spike activity represents both forward prediction and feedback error-related signals, consistent with an involvement of the cerebellum in the prediction of expected sensorimotor states and the detection and correction of motor errors ; for a recent review, see Ebner et

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Section: Synchrony Of Purkinje Cells Can Elicit Time-locked Spiking Imentioning

confidence: 99%

The Neuronal Code(s) of the Cerebellum

et al. 2013

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“…To our knowledge, however, no voltage-clamp studies have been published of the intrinsic currents that produce the firing patterns of these neurons. The spontaneous activity of cerebellar nuclear neurons is particularly interesting because they are the primary targets of Purkinje neurons, which not only are inhibitory (Ito et al, 1970), but themselves fire spontaneous high-frequency action potentials (ϳ50 Hz; Häusser and Clark, 1997;Nam and Hockberger, 1997;. Thus the observed spontaneous firing of cerebellar nuclear neurons apparently persists even during what must be a considerable barrage of inhibition.…”

Section: Abstract: Deep Cerebellar Nuclei; Pacemaking; Action Potentmentioning

confidence: 99%

Ionic Currents and Spontaneous Firing in Neurons Isolated from the Cerebellar Nuclei

2000

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Neurons of the cerebellar nuclei fire spontaneous action potentials both in vitro, with synaptic transmission blocked, and in vivo, in resting animals, despite ongoing inhibition from spontaneously active Purkinje neurons. We have studied the intrinsic currents of cerebellar nuclear neurons isolated from the mouse, with an interest in understanding how these currents generate spontaneous activity in the absence of synaptic input as well as how they allow firing to continue during basal levels of inhibition. Current-clamped isolated neurons fired regularly (ϳ20 Hz), with shallow interspike hyperpolarizations (approximately Ϫ60 mV), much like neurons in more intact preparations. The spontaneous firing frequency lay in the middle of the dynamic range of the neurons and could be modulated up or down with small current injections.During step or action potential waveform voltage-clamp commands, the primary current active at interspike potentials was a tetrodotoxin-insensitive (TTX), cesium-insensitive, voltageindependent, cationic flux carried mainly by sodium ions. Although small, this cation current could depolarize neurons above threshold voltages. Voltage-and current-clamp recordings suggested a high level of inactivation of the TTX-sensitive transient sodium currents that supported action potentials. Blocking calcium currents terminated firing by preventing repolarization to normal interspike potentials, suggesting a significant role for K(Ca) currents. Potassium currents that flowed during action potential waveform voltage commands had high activation thresholds and were sensitive to 1 mM TEA. We propose that, after the decay of high-threshold potassium currents, the tonic cation current contributes strongly to the depolarization of neurons above threshold, thus maintaining the cycle of firing.

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“…1E). All DCN cells receive GABAergic monosynaptic inhibition from Purkinje cells (Ito et al, 1970), indicating the suitability of this system. Monosynaptic IPSPs could be evoked in all of the recorded DCN neurons (n ϭ 10) before gabazine injection (one example illustrated in Fig.…”

Section: Resultsmentioning

confidence: 92%