The olivocerebellar system. I. Delayed and slow inhibitory effects: An overlooked salient feature of cerebellar climbing fibers

Colin, Fabienne; Manil, Jacqueline; Desclin, Jean

doi:10.1016/0006-8993(80)90491-6

Cited by 220 publications

(108 citation statements)

References 74 publications

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“…Our data emphasize the importance of low rates of IO discharge for ongoing motor control: Without that discharge, the simple spike rate of the Purkinje cell rapidly increases to a high rate (Colin et al, 1980), which eliminates output from the cerebellum. Conversely, slightly higher rates of IO discharge eliminate simple spikes (Colin et al, 1980;Rawson and Tilokskulchai, 1981;Montarolo et al, 1982;Strata and Montarolo, 1982); a remarkably small change in complex spike rate controls the total range of simple spike rate.…”

Section: Function Of the Inferior Olivementioning

confidence: 64%

“…Despite the low rate, climbing fiber discharge strongly influences Purkinje cell simple spike discharge, and elimination of olivary input causes simple spike discharge to rapidly increase to a high regular rate (Colin et al, 1980;Rawson and Tilokskulchai, 1981;Montarolo et al, 1982;Strata and Montarolo, 1982). Simple spike discharge inhibits cerebellar nuclear cells (Ito et al, 1964), so a high rate of simple spike discharge effectively turns off cells in the cerebellar nuclei (Benedetti et al, 1983), which reduces discharge in cerebellar targets such as the magnocellular red nucleus (RNm) (Bardin et al, 1983;Billard and Daniel, 1985).…”

Section: Introductionmentioning

confidence: 99%

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Functional Relations of Cerebellar Modules of the Cat

Horn¹,

Pong²,

Gibson³

2010

Journal of Neuroscience

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The cerebellum consists of parasagittal zones that define fundamental modules of neural processing. Each zone receives input from a distinct subdivision of the inferior olive (IO)-activity in one olivary subdivision will affect activity in one cerebellar module. To define functions of the cerebellar modules, we inactivated specific olivary subdivisions in six male cats with a glutamate receptor blocker. Olivary inactivation eliminates Purkinje cell complex spikes, which results in a high rate of Purkinje cell simple spike discharge. The increased simple spike discharge inhibits output from connected regions of the cerebellar nuclei. After inactivation, behavior was evaluated during a reach-to-grasp task and during locomotion. Inactivation of each subdivision produced unique behavioral deficits. Performance of the reach-to-grasp task was affected by inactivation of the rostral dorsal accessory olive (rDAO) and the rostral medial accessory olive (rMAO) and, possibly, the principal olive. rDAO inactivation produced paw drag during locomotion and a deficit in grasping the handle during the reach-to-grasp task. rMAO inactivation caused the cats to reach under the handle and produced severe limb drag during locomotion. Inactivation of the dorsal medial cell column, cell group ␤, or caudal medial accessory olive produced little deficit in the reach-to-grasp task, but each produced a different deficit during locomotion. In all cases, the cats appeared to have intact sensation, good spatial awareness, and no change of affect. Normal cerebellar function requires low rates of IO discharge, and each cerebellar module has a specific and unique function in sensory-motor integration.

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Section: Function Of the Inferior Olivementioning

confidence: 64%

Section: Introductionmentioning

confidence: 99%

Functional Relations of Cerebellar Modules of the Cat

Horn¹,

Pong²,

Gibson³

2010

Journal of Neuroscience

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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).…”

Section: Functions Of Climbing Fiber Burstsmentioning

confidence: 99%

“…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. Such a function, if it exists, may also complement the role of climbing fibers in regulating the level of Purkinje cell simple spike firing (Colin et al, 1980;Cerminara and Rawson, 2004).…”

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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“…If multiple climbing fiber innervation enhances the induction of pf-Pk LTD in vivo, that could lead to an enhanced inhibitory response of the Purkinje cells to the conditioned stimulus, enhanced disinhibition of interpositus neurons, and hence facilitation of blink responses (i.e., enhanced eyeblink conditioning). Likewise, because climbing fiber activity can suppress simple spike activity in the Purkinje cells (Colin et al, 1980;Demer et al, 1985;Luebke and Robinson, 1994), any enhancement in the rate of climbing fiber input to the Purkinje cells attributable to multiple climbing fiber innervation could suppress spontaneous simple spiking in the Purkinje cells, which would also disinhibit the interpositus nucleus and facilitate the production of blinks.…”

Section: Inhibitory and Excitatory Signaling In Cerebellar Circuitsmentioning

confidence: 99%

Impaired Motor Learning in the Vestibulo-Ocular Reflex in Mice with Multiple Climbing Fiber Input to Cerebellar Purkinje Cells

Kimpo

Raymond²

2007

J. Neurosci.

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A unique feature of the cerebellar architecture is that Purkinje cells in the cerebellar cortex each receive input from a single climbing fiber. In mice deficient in the ␥ isoform of protein kinase C (PKC␥ Ϫ/Ϫ mice), this normal architecture is disrupted so that individual Purkinje cells receive input from multiple climbing fibers. These mice have no other known abnormalities in the cerebellar circuit. Here, we show that PKC␥ Ϫ/Ϫ mice are profoundly impaired in vestibulo-ocular reflex (VOR) motor learning. The PKC␥ Ϫ/Ϫ mice exhibited no adaptive increases or decreases in VOR gain at training frequencies of 2 or 0.5 Hz. This impairment was present across a broad range of peak retinal slip speeds during training. We compare the results for VOR motor learning with previous studies of the performance of PKC␥ Ϫ/Ϫ mice on other cerebellum-dependent learning tasks. Together, the results suggest that single climbing fiber innervation of Purkinje cells is critical for some, but not all, forms of cerebellum-dependent learning, and this may depend on the region of the cerebellum involved, the organization of the relevant neural circuits downstream of the cerebellar cortex, as well as the timing requirements of the learning task.

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The olivocerebellar system. I. Delayed and slow inhibitory effects: An overlooked salient feature of cerebellar climbing fibers

Cited by 220 publications

References 74 publications

Functional Relations of Cerebellar Modules of the Cat

Functional Relations of Cerebellar Modules of the Cat

Intraburst and Interburst Signaling by Climbing Fibers

Impaired Motor Learning in the Vestibulo-Ocular Reflex in Mice with Multiple Climbing Fiber Input to Cerebellar Purkinje Cells

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