GABAergic modulation of complex spike activity by the cerebellar nucleoolivary pathway in rat

Lang, Eric J.; Sugihara, Izumi; Llinás, Rodolfó R.

doi:10.1152/jn.1996.76.1.255

Cited by 221 publications

(221 citation statements)

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“…4c), spiking became almost synchronous, and, as in the uncoupled case, the cells generated only regular somatic spikes (firing rate: 3.5 spikes per sec). This increase in synchrony, rhythmicity, and firing rate is consistent with biological data under conditions of increased coupling strengths (22).…”

Section: Moderate Coupling Leads To Chaotic Spiking In Heterogeneous supporting

confidence: 89%

“…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: 88%

“…Our results offer an explanation to the seemingly contradictory reports on rhythmic (21,22) or arhythmic (29) IO neuron firing. It is known that the coupling strength is under control of ␥-aminobutyric acid (GABA)ergic innervation that originates from the cerebellar nuclei (22).…”

Section: Moderate Coupling Leads To Chaotic Spiking In Heterogeneous supporting

confidence: 53%

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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.

113

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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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Section: Moderate Coupling Leads To Chaotic Spiking In Heterogeneous supporting

confidence: 89%

supporting

confidence: 88%

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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.

113

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“…One possibility is that IO neurons may be under increased inhibition from GABAergic afferents, because GABAergic activity not only decreases IO activity but also decouples IO neurons (Lang 2002;Lang et al 1996). Consistent with this possibility, the average CS firing rates of md rats (0.91 Ϯ 0.06 Hz; n ϭ 127) was reduced (17%) compared with the wt rats (1.10 Ϯ 0.05 Hz; n ϭ 243).…”

Section: Cs Synchrony Levels Are Reduced In MD Rats Relative To Wt Ratsmentioning

confidence: 77%

Role of Myelination in the Development of a Uniform Olivocerebellar Conduction Time

Lang¹,

Rosenbluth

2003

Journal of Neurophysiology

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Lang, Eric J. and Jack Rosenbluth. Role of myelination in the development of a uniform olivocerebellar conduction time. J Neurophysiol 89: 2259 -2270, 2003. First published December 18, 2002 10.1152/jn.00922.2002. Purkinje cells generate simultaneous complex spikes as a result of olivocerebellar activity. This synchronization (to within 1 ms) is thought to result from electrotonic coupling of inferior olivary neurons. However, the distance from the inferior olive (IO) varies across the cerebellar cortex. Thus signals generated simultaneously at the IO should arrive asynchronously across the cerebellar cortex, unless the length differences are compensated for. Previously, it was shown that the conduction time from the IO to the cerebellar cortex remains nearly constant at Ϸ4 ms in the rat, implying the existence of such compensatory mechanisms. Here, we examined the role of myelination in generating a constant olivocerebellar conduction time by investigating the latency of complex spikes evoked by IO stimulation during development in normal rats and myelin-deficient mutants. In normal rats, myelination not only reduced overall olivocerebellar conduction time, but also disproportionately reduced the conduction time to vermal lobules, which had the longest response latencies prior to myelination. The net result was a nearly uniform conduction time. In contrast, in myelin-deficient rats, conduction time differences to different parts of the cerebellum remained during the same developmental period. Thus myelination is the primary factor in generating a uniform olivocerebellar conduction time. To test the importance of a uniform conduction time for generating synchronous complex spike activity, multiple electrode recordings were obtained from normal and myelin-deficient rats. Average synchrony levels were higher in normal rats than mutants. Thus the uniform conduction time achieved through myelination of olivocerebellar fibers appears to be essential for the normal expression of complex spike synchrony. I N T R O D U C T I O NInferior olivary (IO) neurons are electrotonically coupled via numerous gap junctions (Llinás and Yarom 1981;Llinás et al. 1974;Sotelo et al. 1974). Indeed, the density of neuronal gap junctions appears to be higher in the IO than in any other CNS region (Belluardo et al. 2000;Condorelli et al. 1998;De Zeeuw et al. 1995). This coupling allows IO neurons to generate precisely (on a millisecond time scale) synchronized activity that results in simultaneous complex spike (CS) activity in the cerebellum (Lang et al. 1999;Sasaki et al. 1989;Sugihara et al. 1993;Yamamoto et al. 2001).Maintenance of the synchronization present in IO discharges presents a challenge for the olivocerebellar system because the length of the olivocerebellar pathway to different points on the cerebellar cortex varies. In rats, there can be more than a twofold difference in the length of the olivocerebellar projection to different regions of the cortex (Sugihara et al. 1993). To preserve the precise synchronization present at...

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“…The rhythmic discharge in long-latency climbing fiber responses is produced by oscillations in the membrane voltage of electrically coupled inferior olivary neurons. Segregation of response patterns following stimulation and the synchronized rhythmicity among multiple olivary neurons are regulated by inhibitory feedback from the cerebellum (Bloedel & Ebner, 1984;Lang, Sugihara, & Llinas, 1996;Llinas, 1974;Llinas, Baker, & Sotelo, 1974;Llinas & Sasaki, 1989;Llinas & Yarom, 1981a, 1981b, 1986. Climbing fiber activity in developing rats was monitored to determine whether inhibition from cerebellar feedback and excitation from sensory input within the inferior olive exhibit ontogenetic changes that correspond to the developmental time course of eyeblink conditioning.…”

Section: Us Pathway Developmentmentioning

confidence: 99%

Developmental Changes in the Neural Mechanisms of Eyeblink Conditioning

Freeman

Nicholson²

2004

Behavioral and Cognitive Neuroscience Reviews

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Eyeblink conditioning has been used as a model system for examining the ontogeny of associative learning and its neural basis in rodents. Associative eyeblink conditioning emerges between postnatal days (P) 17 and 24 in rats. Neurophysiological studies in infant rats during eyeblink conditioning revealed developmental changes in the activity of cerebellar neurons that correspond to the ontogenetic emergence of eyeblink conditioning. The developmental changes in cerebellar neuronal activity suggest that the ontogeny of eyeblink conditioning is related to changes in learning mechanisms rather than motor performance mechanisms. Additional neurophysiological and neuroanatomical studies demonstrated that the developmental changes in neuronal activity in the cerebellum are due to developmental changes in interactions between the cerebellum and its inputs, the inferior olive and pontine nuclei. Developmental changes in cerebellar inputs and regulation of its inputs affect the induction of learning-related plasticity, thereby affecting the rate and magnitude of conditioning.

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GABAergic modulation of complex spike activity by the cerebellar nucleoolivary pathway in rat

Cited by 221 publications

References 0 publications

Chaos may enhance information transmission in the inferior olive

Chaos may enhance information transmission in the inferior olive

Role of Myelination in the Development of a Uniform Olivocerebellar Conduction Time

Developmental Changes in the Neural Mechanisms of Eyeblink Conditioning

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