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

Person, Abigail L.; Raman, Indira M.

doi:10.1038/nature10732

Cited by 315 publications

(426 citation statements)

References 31 publications

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“…It is known from in vivo imaging and multielectrode array measurements that temporally correlated complex spikes occur in parasagittally oriented modules of PNs within the cerebellar cortex (40)(41)(42)(43), and recent evidence is consistent with the idea that the CF-associated teaching signal is encoded by temporally correlated complex spike activity (44). The axons of PNs are inhibitory and converge on single DCN neurons, thus prolonged post-CxSp pauses occurring synchronously in a module of PNs could provide an extended window of disinhibition to the DCN cells receiving such input (45,46). This pattern of activity would have appropriate properties for driving long-term potentiation in mossy fiber-to-DCN synapses (47).…”

Section: Discussionmentioning

confidence: 60%

Prolonging the postcomplex spike pause speeds eyeblink conditioning

Maiz

Karakossian

Pakaprot

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Climbing fiber input to the cerebellum is believed to serve as a teaching signal during associative, cerebellum-dependent forms of motor learning. However, it is not understood how this neural pathway coordinates changes in cerebellar circuitry during learning. Here, we use pharmacological manipulations to prolong the postcomplex spike pause, a component of the climbing fiber signal in Purkinje neurons, and show that these manipulations enhance the rate of learning in classical eyelid conditioning. Our findings elucidate an unappreciated aspect of the climbing fiber teaching signal, and are consistent with a model in which convergent postcomplex spike pauses drive learning-related plasticity in the deep cerebellar nucleus. They also suggest a physiological mechanism that could modulate motor learning rates.associative learning | pavlovian | ZD 7288 | 1-EBIO | rebound

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Section: Discussionmentioning

confidence: 60%

Prolonging the postcomplex spike pause speeds eyeblink conditioning

Maiz

Karakossian

Pakaprot

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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“…S4). Taken these data show that illumination of PCs allows a dynamic control of CN firing (24) and that the duration of inhibition increases with the intensity and duration of light stimulations. Because PC inhibition has been proposed to produce a rebound excitation in CN neurons (25), we examined whether the instantaneous frequency was significantly enhanced relative to baseline values when the cells resumed their firing.…”

Section: Significancementioning

confidence: 77%

Clusters of cerebellar Purkinje cells control their afferent climbing fiber discharge

Chaumont

Guyon

Valera

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

128

137

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Climbing fibers, the projections from the inferior olive to the cerebellar cortex, carry sensorimotor error and clock signals that trigger motor learning by controlling cerebellar Purkinje cell synaptic plasticity and discharge. Purkinje cells target the deep cerebellar nuclei, which are the output of the cerebellum and include an inhibitory GABAergic projection to the inferior olive. This pathway identifies a potential closed loop in the olivo-cortico-nuclear network. Therefore, sets of Purkinje cells may phasically control their own climbing fiber afferents. Here, using in vitro and in vivo recordings, we describe a genetically modified mouse model that allows the specific optogenetic control of Purkinje cell discharge. Tetrode recordings in the cerebellar nuclei demonstrate that focal stimulations of Purkinje cells strongly inhibit spatially restricted sets of cerebellar nuclear neurons. Strikingly, such stimulations trigger delayed climbing-fiber input signals in the stimulated Purkinje cells. Therefore, our results demonstrate that Purkinje cells phasically control the discharge of their own olivary afferents and thus might participate in the regulation of cerebellar motor learning.motor control | olivo-cerebellar loop | complex spikes T he cerebellar cortex is involved in a wealth of functions, from the control of posture to higher cognitive processes (1-3). Purkinje cells (PCs) are key processing units of the cerebellar cortex (4): each PC receives more than 175,000 parallel fiber synaptic inputs carrying information about the ongoing sensorymotor context. It also receives a single inferior olive afferent, the climbing fiber, which triggers a complex spike (CS), modulates PC firing (5), controls synaptic input plasticity, and has been proposed to carry error and clock signals to the cerebellum (2, 4-8). PCs are grouped in multiple parasagittal microzones, each receiving projections from separate areas of the inferior olive and projecting to subregions of the cerebellar nuclei (CN) (9-12). In the CN, PCs make inhibitory contacts on excitatory neurons that project to various premotor areas and propagate cerebellar computations to the motor system. Anatomical evidence indicates that PC terminals also contact CN inhibitory neurons that target inferior olive cells (13,14). This nucleoolivary pathway is topographically organized in multiple parallel projections to the inferior olive subnuclei (15), suggesting the existence of closed olivary-cortico-nuclear loops. Therefore, the discharge of a population of PCs in a microzone might not only shape the output of the cerebellum but also control its afferent climbing-fiber signal. Previous studies have shown that stimulation of the nucleo-olivary pathway significantly reduces olivary cell firing (16-18) and that pharmacological and genetic manipulations of PCs or olivary cell activity induce reciprocal modulations of the firing rate of PCs and climbing fibers (19, 20).These results indicate that PCs may tonically modulate the nucleo-olivary pathway. However, whether...

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“…Complex spike firing is thought to modulate simple spike activity (Barmack and Yakhnitsa 2011). This is important for motor behavior because Purkinje cell firing influences cerebellar nuclear output (Person and Raman 2012). Thus Purkinje cell activity is central to cerebellar function and the control of movement (Badura et al 2013;Chaumont et al 2013;Medina and Lisberger 2008;Popa et al 2013;Witter et al 2013).…”

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confidence: 99%

In vivo analysis of Purkinje cell firing properties during postnatal mouse development

Arancillo

White

Lin

et al. 2015

Journal of Neurophysiology

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Arancillo M, White JJ, Lin T, Stay TL, Sillitoe RV. In vivo analysis of Purkinje cell firing properties during postnatal mouse development. J Neurophysiol 113: 578 -591, 2015. First published October 29, 2014 doi:10.1152/jn.00586.2014.-Purkinje cell activity is essential for controlling motor behavior. During motor behavior Purkinje cells fire two types of action potentials: simple spikes that are generated intrinsically and complex spikes that are induced by climbing fiber inputs. Although the functions of these spikes are becoming clear, how they are established is still poorly understood. Here, we used in vivo electrophysiology approaches conducted in anesthetized and awake mice to record Purkinje cell activity starting from the second postnatal week of development through to adulthood. We found that the rate of complex spike firing increases sharply at 3 wk of age whereas the rate of simple spike firing gradually increases until 4 wk of age. We also found that compared with adult, the pattern of simple spike firing during development is more irregular as the cells tend to fire in bursts that are interrupted by long pauses. The regularity in simple spike firing only reached maturity at 4 wk of age. In contrast, the adult complex spike pattern was already evident by the second week of life, remaining consistent across all ages. Analyses of Purkinje cells in alert behaving mice suggested that the adult patterns are attained more than a week after the completion of key morphogenetic processes such as migration, lamination, and foliation. Purkinje cell activity is therefore dynamically sculpted throughout postnatal development, traversing several critical events that are required for circuit formation. Overall, we show that simple spike and complex spike firing develop with unique developmental trajectories.

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

Cited by 315 publications

References 31 publications

Prolonging the postcomplex spike pause speeds eyeblink conditioning

Prolonging the postcomplex spike pause speeds eyeblink conditioning

Clusters of cerebellar Purkinje cells control their afferent climbing fiber discharge

In vivo analysis of Purkinje cell firing properties during postnatal mouse development

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