Microcircuitry and function of the inferior olive

Zeeuw, Chris I. De; Simpson, J. I.; Hoogenraad, Casper C.; Galjart, Niels; Koekkoek, S.K.E.; Ruigrok, Tom J. H.

doi:10.1016/s0166-2236(98)01310-1

Cited by 419 publications

(318 citation statements)

References 95 publications

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“…This hypothesis is in agreement with the facts that IO neurons are extensively electrically coupled via gap junctions (8) and that IO neurons fire with some degree of rhythmicity and pair-wise synchrony both in vitro (22) and in vivo (21). It is further supported by the general view that electrical junctions synchronize firings of coupled neural oscillators (6,23).…”

supporting

confidence: 89%

“…Third, they exhibit subthreshold oscillations in vitro (5, 6). However, despite this detailed knowledge, we still lack a clear understanding of the function of the cerebellum, and two seemingly contradictory major hypotheses have been proposed, each based on a dramatically different view of the IO (7,8).According to the cerebellar learning hypothesis (9-13), when conjointly activated with parallel fibers, IO spikes modify cerebellar input-output transformations, in agreement with the known long-term depression (LTD) at the parallel fiberPurkinje cell synapse (14). Recent cerebellar motor learning theories (12, 15-19) make two further postulates relevant to this hypothesis.…”

mentioning

confidence: 99%

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Chaos may enhance information transmission in the inferior olive

Schweighofer

Doya

Fukai

et al. 2004

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

119

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Despite unique well characterized neuronal properties, such as extensive electrical coupling and low firing rates, the role of the inferior olive (IO), which is the source of the climbing fiber inputs to cerebellar Purkinje cells, is still controversial. We propose that the IO stochastically recodes the high-frequency information carried by its synaptic inputs into stochastic, low-rate spikes in its climbing fiber output. Computer simulations of realistic IO networks showed that moderate electrical coupling produced chaotic firing, which maximized the input-output mutual information. This ''chaotic resonance'' may allow rich error signals to reach individual Purkinje cells, even at low firing rates, allowing efficient cerebellar learning.O ver a century of cerebellar research has provided us with comprehensive understandings of cerebellar anatomy and physiology. It is well known, for instance, that the output neurons of the cerebellar cortex, the Purkinje cells, receive two major types of synaptic inputs: Ͼ100,000 parallel fibers and a single climbing fiber, an axon from an inferior olive (IO) neuron; whereas summation of parallel fiber inputs generate ''simple spikes,'' a single IO spike generates a ''complex spike'' through the powerful climbing fiber input. Furthermore, the major anatomical and electrophysiological properties of the IO neurons are well characterized (1). First, these neurons generate dendritic and somatic spikes at low firing rates in vivo (three spikes per sec at most) (2). Second, they are electrotonically coupled by gap junctions (3), more extensively than any other cells of the mammalian brain (4). Third, they exhibit subthreshold oscillations in vitro (5, 6). However, despite this detailed knowledge, we still lack a clear understanding of the function of the cerebellum, and two seemingly contradictory major hypotheses have been proposed, each based on a dramatically different view of the IO (7,8).According to the cerebellar learning hypothesis (9-13), when conjointly activated with parallel fibers, IO spikes modify cerebellar input-output transformations, in agreement with the known long-term depression (LTD) at the parallel fiberPurkinje cell synapse (14). Recent cerebellar motor learning theories (12, 15-19) make two further postulates relevant to this hypothesis. First, the IO neurons must fire at a low firing rate so that complex spikes encoding error signals do not interfere with simple spikes carrying motor control commands (12, 15). Second, the IO must transmit error signals (15, 20) with hightemporal resolution for cerebellar learning for efficient motor control.Alternatively, the cerebellar timing hypothesis states that the IO exerts its influence on motor control in real time via synchronous and rhythmic discharges (21). This hypothesis is in agreement with the facts that IO neurons are extensively electrically coupled via gap junctions (8) and that IO neurons fire with some degree of rhythmicity and pair-wise synchrony both in vitro (22) and in vivo (21). It is further support...

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confidence: 89%

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confidence: 99%

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Chaos may enhance information transmission in the inferior olive

Schweighofer

Doya

Fukai

et al. 2004

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

119

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“…Observation that cerebellar lesions can lead to deficits in movement-related timing (Ivry & Keele, 1989;Ivry, Keele, & Diener, 1988) and in non-motor timing at the milliseconds range (Casini & Ivry, 1999) have combined to implicate this structure as a candidate locus for such processes (Ivry, 1996(Ivry, , 1997, but see also (Gibbon et al, 1997). Supporting this idea, network models have shown that the neural architecture of the cerebellum could feasibly measure sub-second intervals in a number of different ways (de Zeeuw et al, 1998;Guigon et al, 1994;Perrett, Ruiz, & Mauk, 1993). Regions of premotor and motor cortex may also be involved in some kinds of time measurement.…”

Section: Activity Greater During the 06 S Intervalmentioning

confidence: 99%

Brain activation patterns during measurement of sub- and supra-second intervals

2003

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The possibility that different neural systems are used to measure temporal durations at the sub-second and several second ranges has been supported by pharmacological manipulation, psychophysics, and neural network modelling. Here, we add to this literature by using fMRI to isolate differences between the brain networks which measure 0.6 and 3 s in a temporal discrimination task with visual discrimination for control. We observe activity in bilateral insula and dorsolateral prefrontal cortex, and in right hemispheric pre-supplementary motor area, frontal pole, and inferior parietal cortex during measurement of both intervals, suggesting that these regions constitute a system used in temporal discrimination at both ranges. The frontal operculum, left cerebellar hemisphere and middle and superior temporal gyri, all show significantly greater activity during measurement of the shorter interval, supporting the hypotheses that the motor system is preferentially involved in the measurement of sub-second intervals, and that auditory imagery is preferentially used during measurement of the same. Only a few voxels, falling in the left posterior cingulate and inferior parietal lobe, are more active in the 3 s condition. Overall, this study shows that although many brain regions are used for the measurement of both sub-and supra-second temporal durations, there are also differences in activation patterns, suggesting that distinct components are used for the two durations.

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“…Much of the intrinsic activity in this network is supported by autonomous subthreshold membrane potential oscillations in IO neurons that display a close-to 10-Hz frequency (5-7). Action potentials in IO neurons occur at the depolarization apex of these oscillations (5).To implement motor coordination via the olivo-cerebellar system, the IO nucleus is organized such that the dendrites of the IO neurons are electrotonically coupled (8, 9) via dendritic gap junctions (10) and receive inhibitory feedback from the cerebellar nuclei (11)(12)(13)(14). It was originally proposed that this inhibitory input produced a dynamic decoupling of the IO neurons (9).…”

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Olivo-cerebellar cluster-based universal control system

Kazantsev

Nekorkin

Makarenko

et al. 2003

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

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The olivo-cerebellar network plays a key role in the organization of vertebrate motor control. The oscillatory properties of inferior olive (IO) neurons have been shown to provide timing signals for motor coordination in which spatio-temporal coherent oscillatory neuronal clusters control movement dynamics. Based on the neuronal connectivity and electrophysiology of the olivo-cerebellar network we have developed a general-purpose control approach, which we refer to as a universal control system (UCS), capable of dealing with a large number of actuator parameters in real time. In this UCS, the imposed goal and the resultant feedback from the actuators specify system properties. The goal is realized through implementing an architecture that can regulate a large number of parameters simultaneously by providing stimuli-modulated spatiotemporal cluster dynamics.T he olivo-cerebellar system, one of the key neuronal circuits in the brain, has been shown to provide highly coordinated signals concerned with the temporal organization of movement execution (1-3). This neuronal network involves inferior olive (IO) neurons whose axons, the climbing fibers, terminate as excitatory inputs onto Purkinje cells in the cerebellar cortex and as en-passant collaterals onto the cerebellar nuclear neurons. The Purkinje cells, in turn, exert a powerful synaptic inhibition onto these cerebellar nuclear neurons (4). Much of the intrinsic activity in this network is supported by autonomous subthreshold membrane potential oscillations in IO neurons that display a close-to 10-Hz frequency (5-7). Action potentials in IO neurons occur at the depolarization apex of these oscillations (5).To implement motor coordination via the olivo-cerebellar system, the IO nucleus is organized such that the dendrites of the IO neurons are electrotonically coupled (8, 9) via dendritic gap junctions (10) and receive inhibitory feedback from the cerebellar nuclei (11)(12)(13)(14). It was originally proposed that this inhibitory input produced a dynamic decoupling of the IO neurons (9). This finding was later demonstrated to be correct by using multiple electrode recordings at the cerebellar cortex (15). Thus, the coupling serves to synchronize the oscillatory phase of IO neurons whereas the return nuclear inhibition, by transiently shunting dendritic coupling, controls cluster size and contour. The interplay between these two processes provides the pattern formation responsible for motor control via ''cluster dynamics'' in the IO (16). Such functional clusters have been demonstrated in vitro by using voltage-dependent dye imaging of the IO (16) and in vivo at the Purkinje cell layer by using multiple electrode recordings (17, 18). The temporal dynamics of the cluster activity have been shown to be directly correlated with premotor temporal patterns of Purkinje cell activity during motor execution (19).The control complexity that the CNS must implement to execute movements as simple as merely grasping an object requires the simultaneous activation of 50 key mu...

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Microcircuitry and function of the inferior olive

Cited by 419 publications

References 95 publications

Chaos may enhance information transmission in the inferior olive

Chaos may enhance information transmission in the inferior olive

Brain activation patterns during measurement of sub- and supra-second intervals

Olivo-cerebellar cluster-based universal control system

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