The olivary input to the cerebellum dissociates sensory events from movement plans

Pi, Jay S.; Sedaghat-Nejad, Ehsan; Fakharian, Mohammad Amin; Hage, Paul; Shadmehr, Reza

doi:10.1101/2022.07.11.499614

Cited by 3 publications

(8 citation statements)

References 100 publications

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“…Thus, the encoding of the sensorimotor space by the climbing fiber input coincided with the downstream effects that the SS suppression had on control of the tongue. Because a similar phenomenon is present among P-cells that contribute to control of the eyes (15,21), our results suggest that across disparate types of movements, the inferior olive imposes a consistent architecture of control upon the cerebellum.…”

Section: Introductionsupporting

confidence: 56%

“…A neuron was identified as a definitive P-cell (n=230) because of the presence of complex spikes (CS). In addition, we included data from putative P-cells (n=54) for which we could not isolate the CSs but the neuron was located in the P-cell layer and exhibited 0 ms synchronous simple spike (SS) interactions with other confirmed P-cells (15,16,25).…”

Section: Resultsmentioning

confidence: 99%

“…We trained head-fixed marmosets to make thousands of tongue movements to harvest food from small tubes that were placed at 90 o to the mouth. We then relied on the fact that the inferior olive not only transmits unexpected sensory events to the cerebellum (12)(13)(14)(15), it also transmits information regarding the direction of the planned movement (15,16). The result is a complex spike that briefly but completely suppresses the P-cell (17,18), resulting in a movement (19), or disruption of the ongoing movement (20,21).…”

Section: Introductionmentioning

confidence: 99%

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Control of tongue movements by the Purkinje cells of the cerebellum

Hage,

Fakharian,

Shoup

et al. 2024

Preprint

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To quantify the cerebellum's contributions to control of the tongue, we trained head-fixed marmosets to make dexterous movements, harvesting food from small tubes that were placed orthogonal to the mouth. We identified the lingual regions in lobule VI of the vermis and recorded from hundreds of Purkinje cells (P-cells), each in sessions where the subject produced thousands of licks. Most movements aimed for one of the small tubes, while other movements groomed the mouth area. To quantify contributions of a P-cell to control of the tongue, we relied on the fact that in a small fraction of the licks, the input from the inferior olive produced a complex spike (CS), which then briefly but completely silenced the P-cell. When the movements were targeting a tube, the CS rates increased during protraction for both ipsilateral and contralateral targets, thus identifying the preferred axis of motion in the olivary input, termed CS-on. However, for grooming movements this modulation was absent. We compared the tongue's trajectory in the targeted movement that had experienced the CS with temporally adjacent targeted licks that had not. When the SS suppression occurred during protraction, the tongue exhibited hypermetria, and when the suppression took place during retraction, the tongue exhibited slowing. These effects amplified when two P-cells were simultaneously suppressed. Therefore, CS-induced suppression of P-cells in the lingual vermis disrupted the forces that would normally decelerate the tongue as it approached the target, demonstrating a specialization in stopping the movement. Because the CS-on direction tended to align with the direction of downstream forces produced during P-cell suppression, this suggests that for targeted licks, the olivary input defined an axis of control for the P-cells.

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Section: Introductionsupporting

confidence: 56%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Control of tongue movements by the Purkinje cells of the cerebellum

Hage,

Fakharian,

Shoup

et al. 2024

Preprint

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“…However, as noted in many experiments, CSs occur not just in response to error, but also before and during a movement (15,(49)(50)(51)(52)(53). Critically, CSs occur before movement onset even when there are no sensory events that triggered that movement (54).…”

Section: Discussionmentioning

confidence: 90%

“…In the oculomotor region of the vermis, each climbing fiber preferentially encodes a particular part of the visual space, but the SSs are modulated for all saccades (12,13). Occasionally, a CS occurs before a saccade, suppressing the SSs that the P-cell would normally produce during that movement (14,15). This allowed us to quantify the relationship between the sensory encoding of the visual space in the climbing fiber input to a P-cell, and the motor consequences of that P-cell's SS suppression.…”

Section: Introductionmentioning

confidence: 99%

Complex spikes perturb movements, revealing the sensorimotor map of Purkinje cells

Muller

Hage

et al. 2023

Preprint

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The cerebellar cortex performs computations that are critical for control of our actions, and then transmits that information via simple spikes of Purkinje cells (P-cells) to downstream structures. However, because P-cells are many synapses away from muscles, we do not know how their output affects behavior. Furthermore, we do not know the level of abstraction, i.e., the coordinate system of the P-cell's output. Here, we recorded spiking activities of hundreds of P-cells in the oculomotor vermis of marmosets during saccadic eye movements and found that following the presentation of a visual stimulus, the olivary input to a P-cell encoded a probabilistic signal that coarsely described both the direction and the amplitude of that stimulus. When this input was present, the resulting complex spike briefly suppressed the P-cell's simple spikes, disrupting the P-cell's output during that saccade. Remarkably, this brief suppression altered the saccade's trajectory by pulling the eyes toward the part of the visual space that was preferentially encoded by the olivary input to that P-cell. Thus, analysis of behavior in the milliseconds following a complex spike unmasked how the P-cell's output influenced behavior: the preferred location in the coordinates of the visual system as conveyed probabilistically from the inferior olive to a P-cell defined the action in the coordinates of the motor system for which that P-cell's simple spikes directed behavior.

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Diversity of the nature of input and output signals in the cerebellum suggests a diversity of function

Orban de Xivry,

Diedrichsen

2024

Current Opinion in Behavioral Sciences

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The olivary input to the cerebellum dissociates sensory events from movement plans

Cited by 3 publications

References 100 publications

Control of tongue movements by the Purkinje cells of the cerebellum

Control of tongue movements by the Purkinje cells of the cerebellum

Complex spikes perturb movements, revealing the sensorimotor map of Purkinje cells

Diversity of the nature of input and output signals in the cerebellum suggests a diversity of function

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