Short-term modulation of cerebellar Purkinje cell activity after spontaneous climbing fiber input

Sato, Yu; Miura, Akira B.; Fushiki, Hiroaki; Kawasaki, Tadashi

doi:10.1152/jn.1992.68.6.2051

Cited by 114 publications

(57 citation statements)

References 18 publications

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“…[42][43][44], the latter phenomenon does not seem to dominate the triggering of the rebound in CN neurons. In addition, these rebounds do not seem to depend on increased activity in long-lasting reverberating loops between CN and precerebellar brainstem nuclei (45,46), because blocking cerebellar output by injecting lidocaine (50-100 nL) at the decussation of the superior cerebellar peduncle (Fig.…”

Section: Resultsmentioning

confidence: 88%

Differential olivo-cerebellar cortical control of rebound activity in the cerebellar nuclei

Hoebeek

Witter

Ruigrok

et al. 2010

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

135

145

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The output of the cerebellar cortex is controlled by two main inputs, (i.e., the climbing fiber and mossy fiber-parallel fiber pathway) and activations of these inputs elicit characteristic effects in its Purkinje cells: that is, the so-called complex spikes and simple spikes. Target neurons of the Purkinje cells in the cerebellar nuclei show rebound firing, which has been implicated in the processing and storage of motor coordination signals. Yet, it is not known to what extent these rebound phenomena depend on different modes of Purkinje cell activation. Using extracellular as well as patch-clamp recordings, we show here in both anesthetized and awake rodents that simple and complex spike-like train stimuli to the cerebellar cortex, as well as direct activation of the inferior olive, all result in rebound increases of the firing frequencies of cerebellar nuclei neurons for up to 250 ms, whereas single-pulse stimuli to the cerebellar cortex predominantly elicit well-timed spiking activity without changing the firing frequency of cerebellar nuclei neurons. We conclude that the rebound phenomenon offers a rich and powerful mechanism for cerebellar nuclei neurons, which should allow them to differentially process the climbing fiber and mossy fiber inputs in a physiologically operating cerebellum.olivo-cerebellar loop | rebound firing | Purkinje cell | complex spikes | simple spikes N eurons in the cerebellar nuclei (CN) form the main output of the cerebellum (1). They include GABAergic neurons that provide an inhibitory feedback to the inferior olive (IO) and excitatory neurons that project to various other brainstem nuclei exerting motor control (2-4). In turn, each CN neuron receives a prominent inhibitory GABAergic input from tens of Purkinje cells, a substantial excitatory input from climbing fiber and mossy fiber collaterals, and a modest input from the local interneurons (4-7). Apart from the impact of these inputs, the firing pattern of CN neurons is largely determined by their intrinsic activities (4,(8)(9)(10)(11)(12)(13)(14). Interestingly, following inhibitory current injections or activation of their Purkinje cell input, CN neurons can show a "rebound" depolarization of the membrane potential, accompanied by action-potential firing (8, 11). Even though little is known about the prominence of rebound firing in the awake state, various models on cerebellar function consider this rebound phenomenon in the nuclei as an essential mechanism to process and store relevant information on motor coordination (15-18). The conductances that allow the rebound firing to emerge involve various types of Ca 2+ -channels, the distribution of which probably varies among the different types of neurons in the CN (8,11,14,(19)(20)(21)(22)(23). Regardless of the type of CN neuron, it is tempting to hypothesize that the climbing fibers and parallel fibers, which evoke complex spikes and simple spikes (24-27), respectively, have a differential impact on the generation of rebound activities in the CN neurons.To test this hypothe...

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Section: Resultsmentioning

confidence: 88%

Differential olivo-cerebellar cortical control of rebound activity in the cerebellar nuclei

Hoebeek

Witter

Ruigrok

et al. 2010

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

135

145

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“…This inactivation, or pause, may be caused both by the direct action of the climbing fiber on the Purkinje cell and by inhibition of the Purkinje cell via activation of the neighboring interneurons through the climbing fiber collaterals (Murphy and Sabah, 1970;Bloedel and Roberts, 1971;Colin et al, 1980). After the pause, the spontaneous simple spike activity of a Purkinje cell may be facilitated, unchanged, or reduced (McDevitt et al, 1982;Sato et al, 1992). The period of inactivation varies from complex spike to complex spike (McDevitt et al, 1982), but, when Purkinje cells are statistically categorized into pause-facilitation, pure-pause, and pause-reduction types, there is a trend associating these cell types with high, medium, and low average frequency of complex spikes, respectively (Sato et al, 1992).…”

Section: Functions Of Climbing Fiber Burstsmentioning

confidence: 99%

“…After the pause, the spontaneous simple spike activity of a Purkinje cell may be facilitated, unchanged, or reduced (McDevitt et al, 1982;Sato et al, 1992). The period of inactivation varies from complex spike to complex spike (McDevitt et al, 1982), but, when Purkinje cells are statistically categorized into pause-facilitation, pure-pause, and pause-reduction types, there is a trend associating these cell types with high, medium, and low average frequency of complex spikes, respectively (Sato et al, 1992). We found a correlation between the average rate of the CFR and the number of EPSP components in a CFR, but whether the number of climbing fiber intraburst spikes plays a role in short-term changes in simple spike activity is not known.…”

Section: Functions Of Climbing Fiber Burstsmentioning

confidence: 99%

Intraburst and Interburst Signaling by Climbing Fibers

Maruta

Hensbroek²,

Simpson³

2007

J. Neurosci.

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Although cerebellar Purkinje cell complex spikes occur at low frequency (ϳ1/s), each complex spike is often associated with a highfrequency burst (ϳ500/s) of climbing fiber spikes. We examined the possibility that signals are present within the climbing fiber bursts. By intracellularly recording from depolarized, nonspiking Purkinje cells in anesthetized pigmented rabbits, climbing fiber burst patterns were investigated by determining the number of components in the induced compound EPSPs during spontaneous activity and during visual stimulation. For our sample of 43 cells, Ͼ70% of all EPSPs were of the compound type composed of two or three EPSPs. During spontaneous activity, the number of components in each compound EPSP was not related to the latency to the succeeding compound EPSP. Conversely, the number of components in each compound EPSP was related to its latency after the preceding compound EPSP. This latency increased from 0.62 s for one-component EPSPs to 1.69 s for compound EPSPs with four or more components. The effect of visual stimulation on the climbing fiber activity was studied in 19 floccular Purkinje cells whose low-frequency interburst climbing fiber response was modulated by movement about the vertical axis. During sinusoidal oscillation (0.1 Hz, Ϯ10°), compound EPSPs with a larger number of components tended to be more prevalent during movement in the excitatory direction than in the inhibitory direction. Thus, climbing fibers can, in addition to modulation of their low interburst frequency, transmit signals in the form of the number of spikes within each high-frequency burst.

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“…The Purkinje cells are excited subsequently by granule cells through axons which are organized into sheets of parallel fibers [Eccles et al, 1966;Eccles et al, 1966]. The characteristic frequency (on average 30 -40 Hz) of simple spikes mediated by the mossy fiber system can be modulated effectively by the other afferent system, the climbing fibers [Lou and Bloedel, 1992;Sato et al, 1992]. A single afferent climbing fiber makes hundreds or thousands of synaptic contacts with a single Purkinje cell, causing a strong excitatory all-or-none response [Eccles, et al, 1966].…”

Section: Generators Of Cerebellar Signalsmentioning

confidence: 99%

“…A single afferent climbing fiber makes hundreds or thousands of synaptic contacts with a single Purkinje cell, causing a strong excitatory all-or-none response [Eccles, et al, 1966]. Rather large functionally specific groups of climbing fibers may become activated synchronously [Llinas and Yarom, 1986;Sato, et al, 1992], thus form- ing an ideal substrate for neurophysiological detection. Furthermore, inferior olivary nuclei, with intrinsic 6 -10 Hz oscillatory properties [Llinas and Yarom, 1986], may provide climbing fiber input to cerebellum with resultant oscillations at sites and of magnitudes which are determined by the degree of neuronal membrane de-and hyperpolarization caused by preceding parallel fiber activity [Hounsgaard and Mitgaard, 1988].…”

Section: Generators Of Cerebellar Signalsmentioning

confidence: 99%

Anticipatory cerebellar responses during somatosensory omission in man

Tesche¹,

Karhu²

2000

Hum. Brain Mapp.

161

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The traditional view of cerebellum is a structure that modifies and synchronizes elements of motor performance. Recent evidence indicates that human cerebellum is involved in a wide range of nonmotor sensory and cognitive functions. A common feature in these diverse motor and nonmotor tasks may be the capacity of cerebellar neuronal circuits to process and anticipate sensory input with high temporal acuity. We present evidence supporting this hypothesis from measurements of the magnetic field at the scalp evoked by neuronal population activity in human cerebellum. Intermittent electrical stimulation of the finger and the median nerve elicited stimulus-locked cerebellar responses with oscillatory components at 6-12 Hz and 25-35 Hz. Sustained oscillatory activity followed random stimulus omissions, with initiation of cerebellar responses prior to the next overt stimulus. These responses indexed processing of temporal features of somatosensory input independent of motor performance or response. The refractory behavior of the responses suggested that a neuronal trace of the temporal pattern of somatosensory stimulation remained in cerebellar circuits for 2-4 s. The cerebellar activity elicited by violation of an established temporal pattern was enhanced when attention was directed to somatosensory stimuli, in concordance with recent imaging studies suggesting participation of cerebellum in attentional networks. The attentional enhancement of the cerebellar responses supports the salience of cerebellar activity in the processing of purely somatosensory input. The short-term maintenance of cerebellar templates for predictable sensory input may reflect a physiological substrate for fine-grained temporal tuning and optimization of performance in large-scale sensory and integrative systems.

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Short-term modulation of cerebellar Purkinje cell activity after spontaneous climbing fiber input

Cited by 114 publications

References 18 publications

Differential olivo-cerebellar cortical control of rebound activity in the cerebellar nuclei

Differential olivo-cerebellar cortical control of rebound activity in the cerebellar nuclei

Intraburst and Interburst Signaling by Climbing Fibers

Anticipatory cerebellar responses during somatosensory omission in man

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