Behavior of floccular Purkinje cells correlated with adaptation of vestibulo-ocular reflex in pigmented rabbits

Nagao, S

doi:10.1007/bf00249606

Cited by 55 publications

(31 citation statements)

References 31 publications

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“…Purkinje cell responses during the VOR, when both head and eye velocity signals contribute to their responses, were shown to be modified in a way that would support motor learning (Watanabe 1984;Nagao 1989). The modification of Purkinje cell responses in the correct direction to support learning may have arisen from brainstem changes by way of the feedback loop shown in Figure 1C (black lines), as their latencies suggested (Lisberger et al 1994a).…”

Section: Evidence For Sites Of Learning and Memorymentioning

confidence: 96%

Learning in a Simple Motor System

Broussard¹,

Kassardjian²

2004

Learn. Mem.

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Motor learning is a very basic, essential form of learning that appears to share common mechanisms across different motor systems. We evaluate and compare a few conceptual models for learning in a relatively simple neural system, the vestibulo-ocular reflex (VOR) of vertebrates. We also compare the different animal models that have been used to study the VOR. In the VOR, a sensory signal from the semicircular canals is transformed into a motor signal that moves the eyes. The VOR can modify the transformation under the guidance of vision. The changes are persistent and share some characteristics with other types of associative learning. The cerebellar cortex is directly linked to the VOR reflex circuitry in a partnership that is present in all vertebrates, and which is necessary for motor learning. Early theories of Marr, Albus, and Ito, in which motor memories are stored solely in the cerebellar cortex, have not explained the bulk of the experimental data. Many studies appear to indicate a site of learning in the vestibular nuclei, and the most successful models have incorporated long-term memory storage in both the cerebellar cortex and the brainstem. Plausible cellular mechanisms for learning have been identified in both structures. We propose that short-term motor memory is initially stored in the cerebellar cortex, and that during consolidation of the motor memory the locus of storage shifts to include a brainstem site. We present experimental results that support our hypothesis.In many situations, inaccurate movements are worse than useless. If the movement is slow, errors can be corrected online by visual or other sensory feedback. However, rapid movements must be intrinsically accurate. This could be accomplished by hard-wiring an accurate movement, which has the obvious disadvantage that the movement cannot be readjusted for changes in downstream motor centers or (in the case of a reflex) for changes in sensory sensitivity. A better solution is to calibrate the movement by trial and error, that is, by motor learning. For our purposes, motor learning is defined as the process by which we acquire precise, coordinated movements, like those that are required in order to run, serve a tennis ball, and type accurately. Because accurate movements are necessary whenever predators must be avoided or prey captured, we can speculate that motor learning may have been one of the earliest types of associative learning to evolve. It has been demonstrated in the ventral nerve cord of insects (Horridge 1962) and is probably universal in freely-moving animals. Furthermore, because its substrate can be relatively simple and well understood, there is a real possibility of understanding motor learning both on the molecular level and on the level of brain circuitry.Motor learning is classified as procedural learning. Errors are monitored and used to guide adaptive changes without conscious awareness. Instead of learning a concept, the subject learns an accurate and appropriate motor response. Distinctions have also been made b...

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Section: Evidence For Sites Of Learning and Memorymentioning

confidence: 96%

Learning in a Simple Motor System

Broussard¹,

Kassardjian²

2004

Learn. Mem.

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“…Surgical lesions, pharmacological inactivation, and genetic disruption of the cerebellum all abolish the ability to adaptively modify VOR gain (Ito et al 1982a, Koekkoek et al 1997, Lisberger et al 1984, Luebke & Robinson 1994, McElligott et al 1998, Michnovicz & Bennett 1987, Nagao 1983, Rambold et al 2002, Robinson 1976, and Purkinje cells exhibit altered responses during the performance of the VOR after motor learning (Hirata & Highstein 2001, Lisberger et al 1994a, Nagao 1989, Watanabe 1984). On the basis of what is known about the contribution of Purkinje cells to eye movements, the responses of Purkinje cells during the VOR change in the correct direction to contribute to the altered eye movement response to head movement.…”

Section: Role Of the Cerebellum In Motor Learning In The Vor: Two Infmentioning

confidence: 97%

CEREBELLUM-DEPENDENT LEARNING: The Role of Multiple Plasticity Mechanisms

Boyden

Katoh

Raymond

2004

Annu. Rev. Neurosci.

412

306

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The cerebellum is an evolutionarily conserved structure critical for motor learning in vertebrates. The model that has influenced much of the work in the field for the past 30 years suggests that motor learning is mediated by a single plasticity mechanism in the cerebellum: long-term depression (LTD) of parallel fiber synapses onto Purkinje cells. However, recent studies of simple behaviors such as the vestibulo-ocular reflex (VOR) indicate that multiple plasticity mechanisms contribute to cerebellum-dependent learning. Multiple plasticity mechanisms may provide the flexibility required to store memories over different timescales, regulate the dynamics of movement, and allow bidirectional changes in movement amplitude. These plasticity mechanisms must act in combination with appropriate information-coding strategies to equip motor-learning systems with the ability to express learning in correct contexts. Studies of the patterns of generalization of motor learning in the VOR provide insight about the coding of information in neurons at sites of plasticity. These principles emerging from studies of the VOR are consistent with results concerning more complex behaviors and thus may reflect general principles of cerebellar function.

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“…VOR is a reflex to turn an eyeball in the opposite direction of head turn, and works to stabilize visual image during head motion (Robinson, 1981). VOR undergoes adaptive modification in the direction to reduce image slip on a retina, which has been regarded as a model paradigm of cerebellum-dependent motor learning (Ito, 1982, 2011; Nagao, 1989; Lisberger et al, 1994; du Lac et al, 1995; Hirata and Highstein, 2001; Katoh et al, 2005; Hirano, 2013a). In experiments, a mouse is rotated sinusoidally on a rotating table, and a surrounding external screen with vertical black and white stripes is also rotated simultaneously (Tanaka et al, 2013).…”

Section: Involvement Of Rebound Potentiation (Rp) In Motor Learningmentioning

confidence: 99%

Regulation and functional roles of rebound potentiation at cerebellar stellate cell—Purkinje cell synapses

Hirano

Kawaguchi

2014

Front. Cell. Neurosci.

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Purkinje cells receive both excitatory and inhibitory synaptic inputs and send sole output from the cerebellar cortex. Long-term depression (LTD), a type of synaptic plasticity, at excitatory parallel fiber–Purkinje cell synapses has been studied extensively as a primary cellular mechanism of motor learning. On the other hand, at inhibitory synapses on a Purkinje cell, postsynaptic depolarization induces long-lasting potentiation of GABAergic synaptic transmission. This synaptic plasticity is called rebound potentiation (RP), and its molecular regulatory mechanisms have been studied. The increase in intracellular Ca2+ concentration caused by depolarization induces RP through enhancement of GABAA receptor (GABAAR) responsiveness. RP induction depends on binding of GABAAR with GABAAR associated protein (GABARAP) which is regulated by Ca2+/calmodulin-dependent kinase II (CaMKII). Whether RP is induced or not is determined by the balance between phosphorylation and de-phosphorylation activities regulated by intracellular Ca2+ and by metabotropic GABA and glutamate receptors. Recent studies have revealed that the subunit composition of CaMKII has significant impact on RP induction. A Purkinje cell expresses both α- and β-CaMKII, and the latter has much higher affinity for Ca2+/calmodulin than the former. It was shown that when the relative amount of α- to β-CaMKII is large, RP induction is suppressed. The functional significance of RP has also been studied using transgenic mice in which a peptide inhibiting association of GABARAP and GABAAR is expressed selectively in Purkinje cells. The transgenic mice show abrogation of RP and subnormal adaptation of vestibulo-ocular reflex (VOR), a type of motor learning. Thus, RP is involved in a certain type of motor learning.

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Behavior of floccular Purkinje cells correlated with adaptation of vestibulo-ocular reflex in pigmented rabbits

Cited by 55 publications

References 31 publications

Learning in a Simple Motor System

Learning in a Simple Motor System

CEREBELLUM-DEPENDENT LEARNING: The Role of Multiple Plasticity Mechanisms

Regulation and functional roles of rebound potentiation at cerebellar stellate cell—Purkinje cell synapses

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