Translational Approach to Behavioral Learning: Lessons from Cerebellar Plasticity

Chéron, Guy; Dan, Bernard; Márquez-Ruiz, Javier

doi:10.1155/2013/853654

Cited by 20 publications

(23 citation statements)

References 211 publications

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“…The effects of DIN and IO ablation on H-reflex down-conditioning are consistent with current ideas about the role of the cerebellum and IO in other simple motor skills (Martin et al 1996;Boyden et al 2004;Thompson, 2005;Freeman & Steinmetz, 2011;Cheron et al 2013;Longley & Yeo, 2014). Vestibuloocular reflex conditioning and eyeblink conditioning are thought to involve cerebellar plasticity caused by the conjunction of activity in specific mossy and climbing fibres, with the climbing fibres, which originate in the IO, providing a teaching signal (Boyden et al 2004;Thompson, 2005;Welsh et al 2005;Freeman & Steinmetz, 2011;Schonewille et al 2011;Cheron et al 2013;Longley & Yeo, 2014;Mauk et al 2014). A similar conjunction could underlie H-reflex conditioning.…”

Section: A Simple Motor Behaviour: the Reflex Operant Conditioning supporting

confidence: 68%

“…2004; Thompson, ; Freeman & Steinmetz, ; Cheron et al . 2013; Longley & Yeo, ). Vestibuloocular reflex conditioning and eyeblink conditioning are thought to involve cerebellar plasticity caused by the conjunction of activity in specific mossy and climbing fibres, with the climbing fibres, which originate in the IO, providing a teaching signal (Boyden et al .…”

Section: Evidence Supporting the Modelmentioning

confidence: 99%

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The negotiated equilibrium model of spinal cord function

Wolpaw

2018

The Journal of Physiology

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The belief that the spinal cord is hardwired is no longer tenable. Like the rest of the CNS, the spinal cord changes during growth and ageing, when new motor behaviours are acquired, and in response to trauma and disease. This paper describes a new model of spinal cord function that reconciles its recently appreciated plasticity with its long‐recognized reliability as the final common pathway for behaviour. According to this model, the substrate of each motor behaviour comprises brain and spinal plasticity: the plasticity in the brain induces and maintains the plasticity in the spinal cord. Each time a behaviour occurs, the spinal cord provides the brain with performance information that guides changes in the substrate of the behaviour. All the behaviours in the repertoire undergo this process concurrently; each repeatedly induces plasticity to preserve its key features despite the plasticity induced by other behaviours. The aggregate process is a negotiation among the behaviours: they negotiate the properties of the spinal neurons and synapses that they all use. The ongoing negotiation maintains the spinal cord in an equilibrium – a negotiated equilibrium – that serves all the behaviours. This new model of spinal cord function is supported by laboratory and clinical data, makes predictions borne out by experiment, and underlies a new approach to restoring function to people with neuromuscular disorders. Further studies are needed to test its generality, to determine whether it may apply to other CNS areas such as the cerebral cortex, and to develop its therapeutic implications.

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Section: A Simple Motor Behaviour: the Reflex Operant Conditioning supporting

confidence: 68%

Section: Evidence Supporting the Modelmentioning

confidence: 99%

The negotiated equilibrium model of spinal cord function

Wolpaw

2018

The Journal of Physiology

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“…Given the cardinal learning impairments and cerebellar dysfunction in AS, the role of cerebellar plasticity has attracted increasing attention. The specific relationship between cerebellar cortex and inferior olive has recently been suggested to provide an informative avenue for integrating the evidences of neuronal plasticity in a translational perspective (Cheron et al, 2013 ). The Purkinje cells plastic properties are specifically controlled by input from climbing fibers, allowing processing through both feed-forward and feedback loops inside the cerebellar cortex.…”

Section: Introductionmentioning

confidence: 99%

Disruption of the LTD dialogue between the cerebellum and the cortex in Angelman syndrome model: a timing hypothesis

Chéron

Márquez-Ruiz

Kishino

et al. 2014

Front. Syst. Neurosci.

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Angelman syndrome (AS) is a genetic neurodevelopmental disorder in which cerebellar functioning impairment has been documented despite the absence of gross structural abnormalities. Characteristically, a spontaneous 160 Hz oscillation emerges in the Purkinje cells network of the Ube3am−/p+ Angelman mouse model. This abnormal oscillation is induced by enhanced Purkinje cell rhythmicity and hypersynchrony along the parallel fiber beam. We present a pathophysiological hypothesis for the neurophysiology underlying major aspects of the clinical phenotype of AS, including cognitive, language and motor deficits, involving long-range connection between the cerebellar and the cortical networks. This hypothesis states that the alteration of the cerebellar rhythmic activity impinges cerebellar long-term depression (LTD) plasticity, which in turn alters the LTD plasticity in the cerebral cortex. This hypothesis was based on preliminary experiments using electrical stimulation of the whiskers pad performed in alert mice showing that after a 8 Hz LTD-inducing protocol, the cerebellar LTD accompanied by a delayed response in the wild type (WT) mice is missing in Ube3am−/p+ mice and that the LTD induced in the barrel cortex following the same peripheral stimulation in wild mice is reversed into a LTP in the Ube3am−/p+ mice. The control exerted by the cerebellum on the excitation vs. inhibition balance in the cerebral cortex and possible role played by the timing plasticity of the Purkinje cell LTD on the spike–timing dependent plasticity (STDP) of the pyramidal neurons are discussed in the context of the present hypothesis.

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“…Two other simple learning phenomena, vestibuloocular reflex (VOR) conditioning and eyeblink conditioning, are believed to depend on cerebellar plasticity produced by the conjunction of activity in particular mossy and climbing fibers (Boyden et al 2004;Cheron et al 2013;Freeman and Steinmetz 2011;Longley and Yeo 2014;Mauk et al 2014;Schonewille et al 2011;Thompson 2005;Welsh et al 2005). The climbing fibers, which originate in the IO, are hypothesized to provide a teaching signal.…”

Section: Discussionmentioning

confidence: 99%

Ablation of the inferior olive prevents H-reflex down-conditioning in rats

Chen

Wang

Chen

et al. 2016

Journal of Neurophysiology

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We evaluated the role of the inferior olive (IO) in acquisition of the spinal cord plasticity that underlies H-reflex down-conditioning, a simple motor skill. The IO was chemically ablated before a 50-day exposure to an operant conditioning protocol that rewarded a smaller soleus H-reflex. In normal rats, down-conditioning succeeds (i.e., H-reflex size decreases at least 20%) in 80% of animals. Down-conditioning failed in every IO-ablated rat (P Ͻ 0.001 vs. normal rats). IO ablation itself had no long-term effect on H-reflex size. These results indicate that the IO is essential for acquisition of a down-conditioned H-reflex. With previous data, they support the hypothesis that IO and cortical inputs to cerebellum enable the cerebellum to guide sensorimotor cortex plasticity that produces and maintains the spinal cord plasticity that underlies the down-conditioned H-reflex. They help to further define H-reflex conditioning as a model for understanding motor learning and as a new approach to enhancing functional recovery after trauma or disease. operant conditioning; spinal cord; plasticity; cerebellum; learning EVEN THE SIMPLEST LEARNING produces plasticity at multiple places in the CNS (e.g., Carrier et al. 1997;Lieb and Frost 1997;Longley and Yeo 2014;Wolpaw and Lee 1989). Thus a central challenge in understanding learning is to explain how changes at many sites combine to account for the acquisition and maintenance of a newly learned behavior, and also for the preservation of previously learned behaviors that use some of the same neurons and synapses. Operant conditioning of the H-reflex, an electrical analog of the spinal stretch reflex (e.g., the knee-jerk reflex), provides a unique opportunity to address the challenge. By a standard definition of motor skill as an adaptive behavior acquired through practice (e.g., Shmuelof and Krakauer 2011), operantly conditioned change in the H-reflex is a simple motor skill. This learning changes both the brain and the spinal cord (Wolpaw and Chen 2006; see Thompson and Wolpaw 2014 and Wolpaw 2010 for review). The anatomical separation of the spinal cord from the brain and the direct connection of the spinal cord to behavior (i.e., to muscle activity) facilitate study of the manner in which the spinal and supraspinal plasticity produced by H-reflex conditioning combine to acquire and maintain a smaller (i.e., down-conditioned) or larger (i.e., up-conditioned) H-reflex, while at the same time maintaining other behaviors that use the same spinal circuitry.The studies to date indicate that the corticospinal tract (CST) and cerebellar output to cortex are essential for acquisition of the spinal cord plasticity that is directly responsible for a smaller (i.e., down-conditioned) H-reflex, while other major descending and ascending tracts are not essential (Chen and Wolpaw 1997. The cerebellum might simply be required for the normal functioning of sensorimotor cortex (SMC), or it might actually guide the CST activity that produces the spinal cord plasticity that is directly res...

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Translational Approach to Behavioral Learning: Lessons from Cerebellar Plasticity

Cited by 20 publications

References 211 publications

The negotiated equilibrium model of spinal cord function

The negotiated equilibrium model of spinal cord function

Disruption of the LTD dialogue between the cerebellum and the cortex in Angelman syndrome model: a timing hypothesis

Ablation of the inferior olive prevents H-reflex down-conditioning in rats

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