Climbing fibers predict movement kinematics and performance errors
Open accessAbstract
Requisite for understanding cerebellar function is a complete characterization of the signals provided by complex spike (CS) discharge of Purkinje cells, the output neurons of the cerebellar cortex. Numerous studies have provided insights into CS function, with the most predominant view being that they are evoked by error events. However, several reports suggest that CSs encode other aspects of movements and do not always respond to errors or unexpected perturbations. Here, we evaluated CS firing during a pseudo-random manual tracking task in the monkey ( Macaca mulatta). This task provides extensive coverage of the work space and relative independence of movement parameters, delivering a robust data set to assess the signals that activate climbing fibers. Using reverse correlation, we determined feedforward and feedback CSs firing probability maps with position, velocity, and acceleration, as well as position error, a measure of tracking performance. The direction and magnitude of the CS modulation were quantified using linear regression analysis. The major findings are that CSs significantly encode all three kinematic parameters and position error, with acceleration modulation particularly common. The modulation is not related to “events,” either for position error or kinematics. Instead, CSs are spatially tuned and provide a linear representation of each parameter evaluated. The CS modulation is largely predictive. Similar analyses show that the simple spike firing is modulated by the same parameters as the CSs. Therefore, CSs carry a broader array of signals than previously described and argue for climbing fiber input having a prominent role in online motor control. NEW & NOTEWORTHY This article demonstrates that complex spike (CS) discharge of cerebellar Purkinje cells encodes multiple parameters of movement, including motor errors and kinematics. The CS firing is not driven by error or kinematic events; instead it provides a linear representation of each parameter. In contrast with the view that CSs carry feedback signals, the CSs are predominantly predictive of upcoming position errors and kinematics. Therefore, climbing fibers carry multiple and predictive signals for online motor control.
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An examination of SS firing encoding uncovered that CSs trigger robust, step-like changes in the kinematic and position error signals present in the SS discharge.
“An examination of the SS firing encoding uncovered that CSs trigger robust, step-like changes in the kinematic and position error signals present in the SS discharge.”
From Cerebellum, Predictions and Errors (2019) · cites this paper as Streng et al., 2017
The Discussion says CS occurrence is tightly timed to changes in SS sensitivity to motor parameters and reports earlier work showing that CSs control information encoded in SS firing. The results also show that SS discharge represents kinematics and position error. Our copy does not describe those changes as robust or step-like; it frames climbing-fiber alteration of SS sensitivity as a hypothesis. (LLM, conf=0.83)
Experimental — accuracy not yet measuredPurkinje cell recordings during pseudo-random tracking confirm that SS firing encodes arm movement kinematics including position, velocity, and acceleration.
“Purkinje cell recordings during pseudo-random tracking confirm that SS firing encodes arm movement kinematics including position, velocity, and acceleration (Hewitt et al., 2011; Popa et al., 2012, 2017; Streng et al., 2017).”
From Cerebellum, Predictions and Errors (2019) · cites this paper as Streng et al., 2017
Climbing fiber input signals movement information beyond motor errors.
“Moreover, during pseudo-random tracking CS firing modulates strongly with arm kinematics including position, velocity, and acceleration, showing that climbing fiber input signals movement information beyond motor errors (Streng et al., 2017).”
From Cerebellum, Predictions and Errors (2019) · cites this paper as Streng et al., 2017
During pseudo-random tracking, climbing fiber modulation leads both kinematics and performance errors.
“Although typically thought to be primarily driven by feedback errors, during pseudo-random tracking, climbing fiber modulation leads both kinematics and performance errors (Streng et al., 2017).”
From Cerebellum, Predictions and Errors (2019) · cites this paper as Streng et al., 2017
During pseudo-random tracking, CS firing modulates strongly with arm kinematics including position, velocity, and acceleration.
“Moreover, during pseudo-random tracking CS firing modulates strongly with arm kinematics including position, velocity, and acceleration, showing that climbing fiber input signals movement information beyond motor errors (Streng et al., 2017).”
From Cerebellum, Predictions and Errors (2019) · cites this paper as Streng et al., 2017
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Cerebellum, Predictions and Errors
Popa, L. S., & Ebner, T. J. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00524 · Cited by 191 · see citing works
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- Authors
- Streng, M. L., Popa, L. S., & Ebner, T. J.
- Affiliations
- University of Minnesota (US)
- Corresponding author
- Ebner, Timothy J.
- Venue
- Journal of Neurophysiology
- Publisher
- American Physiological Society
- Published
- 2017-09-01
- Volume
- 118
- Issue
- 3
- Pages
- 1888-1902
- ISSN
- 0022-3077 (ISSN-L)
- 1522-1598
- PMC
- PMC5599663
- OpenAlex
- W2735332171
- Cited by
- 17
- References
- 94
- Citations by year
- 2025: 2 · 2024: 1 · 2023: 1 · 2022: 2 · 2021: 2 · 2019: 5 · 2018: 4
- FWCI
- 1.41
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neurophysiology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- HHS | NIH | National Institute of Neurological Disorders and Stroke (NINDS) (R01 NS18338, F31 NS095408)
- HHS | National Institutes of Health (NIH) (T32 GM008471)
- National Science Foundation (NSF) (IGERT DGE-1069104)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Life Sciences › Neuroscience › Neurology › Vestibular and auditory disorders
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- climbing fibers, complex spikes, Purkinje cells, cerebellum, movement kinematics, positioning error, simple spikes, online motor control, predictive coding, reverse correlation, manual tracking, macaque
- MeSH terms
- Action Potentials, Animals, Biomechanical Phenomena, Female, Macaca mulatta, Male, Motor Skills, Movement, Purkinje Cells, Task Performance and Analysis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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