Cerebellum involvement in cortical sensorimotor circuits for the control of voluntary movements

Proville, Rémi; Spolidoro, Maria; Guyon, Nicolas; Dugué, Guillaume P.; Selimi, Fekrije; Isope, Philippe; Popa, Daniela; Léna, Clément

doi:10.1038/nn.3773

Cited by 222 publications

(237 citation statements)

References 51 publications

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“…One possibility is that precise linkage to movement is a characteristic of particular regions of cerebellar cortex. For example, it has been recently reported that neurons in lateral crus I of the rodent cerebellum respond robustly (<10ms) and selectively to stimulation of whisking-related areas of sensory and motor cortex [16]. We speculate such direct connectivity between sensory inputs/motor outputs, and these specific cerebellar regions is essential for the construction of forward models.…”

Section: Encoding Of Sensory Prediction Errors In the Rostral Fastigimentioning

confidence: 84%

Neural Correlates of Sensory Prediction Errors in Monkeys: Evidence for Internal Models of Voluntary Self-Motion in the Cerebellum

Cullen

Brooks

2014

Cerebellum

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During self-motion, the vestibular system makes essential contributions to postural stability and self-motion perception. To ensure accurate perception and motor control it is critical to distinguish between vestibular sensory inputs that are the result of externally applied motion (exafference) and that are the result of our own actions (reafference). Indeed, although the vestibular sensors encode vestibular afference and reafference with equal fidelity, neurons at the first central stage of sensory processing selectively encode vestibular exafference. The mechanism underlying this reafferent suppression compares the brain's motor-based expectation of sensory feedback with the actual sensory consequences of voluntary self-motion, effectively computing the sensory prediction error (i.e., exafference). It is generally thought that sensory prediction errors are computed in the cerebellum, yet it has been challenging to explicitly demonstrate this. We have recently addressed this question, and found that deep cerebellar nuclei neurons explicitly encode sensory prediction errors during self-motion. Importantly, in everyday life, sensory prediction errors occur in response to changes in the effector /or world (muscle strength, load, etc), as well as in response to externally applied sensory stimulation. Accordingly, we hypothesize that altering the relationship between motor commands and the actual movement parameters will result in the updating in the cerebellum-based computation of exafference. If our hypothesis is correct, under these conditions neuronal responses should initially be increased – consistent with a sudden increase in the sensory prediction error. Then, over time as the internal model is updated, response modulation should decrease in parallel with a reduction in sensory prediction error, until vestibular reafference is again suppressed. The finding that the internal model predicting the sensory consequences of motor commands adapts for new relationships would have important implications for understanding how responses to passive stimulation endure despite the cerebellum's ability to learn new relationships between motor commands and sensory feedback.

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Section: Encoding Of Sensory Prediction Errors In the Rostral Fastigimentioning

confidence: 84%

Neural Correlates of Sensory Prediction Errors in Monkeys: Evidence for Internal Models of Voluntary Self-Motion in the Cerebellum

Cullen

Brooks

2014

Cerebellum

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“…In this case one could imagine that the cortex was excited by the thalamus as it relayed cerebellar information 18,19 . This increased cerebellar-induced cortical activity could then subsequently activate striatal neurons.…”

Section: Resultsmentioning

confidence: 99%

Short latency cerebellar modulation of the basal ganglia

et al. 2014

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The graceful, purposeful motion of our body is an engineering feat which remains unparalleled in robotic devices using advanced artificial intelligence. Much of the information required for complex movements is generated by the cerebellum and the basal ganglia in conjunction with the cortex. Cerebellum and basal ganglia have been thought to communicate with each other only through slow multi-synaptic cortical loops, begging the question as to how they coordinate their outputs in real time. Here we show in mice that the cerebellum rapidly modulates the activity of the striatum via a disynaptic pathway. Under physiological conditions this short latency pathway is capable of facilitating optimal motor control by allowing the basal ganglia to incorporate time-sensitive cerebellar information and by guiding the sign of cortico-striatal plasticity. Conversely, under pathological condition this pathway relays aberrant cerebellar activity to the basal ganglia to cause dystonia.

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“…The majority of nucleocortical collateral axons were found to target cortical regions of the 4 th /5 th lobule shown to receive sensory input from hind and forelimbs in both rats and cats (Provini et al, 1968; Buisseret-Delmas and Angaut, 1993), and the Crus I lobule thought to receive sensory and motor input from the face and vibrissa of mice (Proville et al, 2014). In addition, we located nucleocortical collateral axons targeting a more anterior cortical zone that has been recently identified to participate in eyelid conditioning (Heiney et al, 2014; Steinmetz and Freeman, 2014).…”

Section: Discussionmentioning

confidence: 99%

Cerebellar premotor output neurons collateralize to innervate the cerebellar cortex

Houck

Person

2015

J of Comparative Neurology

101

118

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Motor commands computed by the cerebellum are hypothesized to use corollary discharge, or copies of outgoing commands, to accelerate motor corrections. Identifying sources of corollary discharge, therefore, is critical for testing this hypothesis. Here, we verified that the pathway from the cerebellar nuclei to the cerebellar cortex in mice includes collaterals of cerebellar premotor output neurons, mapped this collateral pathway, and identified its postsynaptic targets. Following bidirectional tracer injections into a distal target of the cerebellar nuclei, the ventrolateral thalamus, we observed retrogradely labeled somata in the cerebellar nuclei and mossy fiber terminals in the cerebellar granule layer, consistent with collateral branching. Corroborating these observations, bidirectional tracer injections into the cerebellar cortex retrogradely labeled somata in the cerebellar nuclei and boutons in the ventrolateral thalamus. To test whether nuclear output neurons projecting to the red nucleus also collateralize to the cerebellar cortex, we used a Cre-dependent viral approach, avoiding potential confounds of direct red nucleus-to-cerebellum projections. Injections of a Cre-dependent GFP-expressing virus into Ntsr1-Cre mice, which express Cre selectively in the cerebellar nuclei, retrogradely labeled somata in the interposed nucleus and putative collateral branches terminating as mossy fibers in the cerebellar cortex. Postsynaptic targets of all labeled mossy fiber terminals were identified using immunohistochemical Golgi cell markers and electron microscopic profiles of granule cells, indicating that the collaterals of nuclear output neurons contact both Golgi and granule cells. These results clarify the organization of a subset of nucleocortical projections which constitute an experimentally accessible corollary discharge pathway within the cerebellum.

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Cerebellum involvement in cortical sensorimotor circuits for the control of voluntary movements

Cited by 222 publications

References 51 publications

Neural Correlates of Sensory Prediction Errors in Monkeys: Evidence for Internal Models of Voluntary Self-Motion in the Cerebellum

Neural Correlates of Sensory Prediction Errors in Monkeys: Evidence for Internal Models of Voluntary Self-Motion in the Cerebellum

Short latency cerebellar modulation of the basal ganglia

Cerebellar premotor output neurons collateralize to innervate the cerebellar cortex

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