Neural Correlates of Sensory Prediction Errors in Monkeys: Evidence for Internal Models of Voluntary Self-Motion in the Cerebellum
Open accessAbstract
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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Claims the paper makes
5 of 19 cited sources checked · 3 supported · 0 flagged · accuracy not yet measured
- Premisecitation
Clinical studies in neurologic patients and brain stimulation studies suggest that cerebellum-dependent mechanisms are involved.
“Furthermore, clinical studies with neurologic patients [4] and using brain stimulation [5] suggest a role for cerebellum-dependent mechanisms.”
Quote in the paperNot a substantial claim1 of 2 sources checked- cites [4] Tseng YW, Diedrichsen J, Krakauer JW, Shadmehr R, Bastian AJ. Sensory prediction errors drive cerebellum-dependent adaptation of reaching. J Neurophysiol. 2007;98:54–62. source
- cites [5] Galea JM, Vazquez A, Pasricha N, de Xivry JJ, Celnik P. Dissociating the roles of the cerebellum and motor cortex during adaptive learning: the motor cortex retains what the cerebellum learns. Cereb Cortex. 2011;21:1761–70. source
- Interpretationcitation
Sensory reafference is suppressed when proprioceptive feedback matches the feedback expected from the motor command.
“Moreover, to date, our experimental evidence is consistent with the proposal that suppression of sensory reafference occurs when proprioceptive feedback matches that expected as a result of the motor command (as during normal active movements) [7, 14].”
Quote in the paperSubstantial claim1 of 2 sources checked- cites [7] Roy JE, Cullen KE. Dissociating self-generated from passively applied head motion: neural mechanisms in the vestibular nuclei. J Neurosci. 2004;24:2102–11. source
- cites [14] Brooks JX, Cullen KE. Early vestibular processing does not discriminate active from passive self-motion if there is a discrepancy between predicted and actual proprioceptive feedback. J Neurophysiol. 2014;111:2465–78. source
- Findingnone given
Fastigial nucleus neuron responses are tightly linked to externally applied self-motion.
“In contrast FN neuron responses are tightly coupled to externally-applied self-motion.”
Quote in the paperNot a substantial claim - Findingown data
When active and passive motion are combined, rostral fastigial nucleus neurons encode only the externally imposed component of the movement.
“Moreover, when active and passive motion occurs simultaneously, the externally applied component of the movement is selectively encoded (Fig. 1B).”
Quote in the paperSubstantial claim - Findingown data
In the rostral fastigial nucleus, neurons that reliably encode passive head and body motion are strongly suppressed during self-generated head and body movements.
“We found that: neurons in the rostral FN that faithfully encode passive head and body motion are greatly suppressed during actively generated movements of the head and body.”
Quote in the paperSubstantial claim
- Interpretationown data
Neurons in the deep cerebellar nuclei carry an explicit signal for sensory prediction errors when an animal moves itself.
“We have recently addressed this question, and found that deep cerebellar nuclei neurons explicitly encode sensory prediction errors during self-motion.”
- Also stated in: § Encoding of sensory prediction errors in the rostral fastigial nucleus · boosted
“These findings show for the first time that neurons in the cerebellum explicitly encode sensory prediction errors detailing the time course of externally applied self-motion.”
Quote in the paperSubstantial claim - Also stated in: § Encoding of sensory prediction errors in the rostral fastigial nucleus · boosted
- Interpretationnone given
Continued suppression of reafference despite sustained changes in the motor command-sensory feedback relationship is essential for the vestibular system's contributions to vestibulo-spinal reflexes and self-motion perception.
“Continued reafference suppression in the face of sustained changes in the relationship between motor commands and sensory feedback is essential the vestibular system's contribution to both vestibulo-spinal reflexes and self-motion perception.”
Quote in the paperNot a substantial claim - Premisecitation
The brain computes a sensory prediction error by comparing a motor-based expectation of sensory feedback against the actual sensory consequences of voluntary self-motion.
“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).”
- Also stated in: § Encoding of sensory prediction errors in the rostral fastigial nucleus · hedged
“It had been proposed that our brain constructs an internal model of the expected sensory consequences of movement based on an efference copy of the self-produced motor command [7].”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [7] Roy JE, Cullen KE. Dissociating self-generated from passively applied head motion: neural mechanisms in the vestibular nuclei. J Neurosci. 2004;24:2102–11. source
- Also stated in: § Encoding of sensory prediction errors in the rostral fastigial nucleus · hedged
- Classified as probably not a substantial claim. 10
- May combine two claims. 4
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationPrevious motor learning studies used catch trials to assess whether an internal model had been updated.
“Furthermore, previous motor learning studies have further used ‘catch trials’ (which refers to removal of the experimentally induced perturbation unexpectedly for single trials during a learning paradigm) as a way to assess whether an internal model has been updated [15].”
Quote in the paperNot a substantial claim1 of 1 sources checked- cites [15] Berniker M, Kording K. Estimating the sources of motor errors for adaptation and generalization. Nat Neurosci. 2008;11:1454–61. source
The Results (Inertial disturbance studies; page unavailable) describe aftereffects when a perturbation is removed, consistent with using removal to reveal adaptation. But our copy does not say that previous studies used catch trials—unexpected, single-trial removals during learning—to assess internal-model updates (searched: catch trials, single-trial removal). (LLM, conf=0.82)
Experimental — accuracy not yet measured
Classified as probably not a substantial claim.
PremisecitationIf the behavioral response to catch trials is the mirror image of the initial perturbation-induced change, this indicates that the motor system incorporated the perturbation into its internal motor plan and updated its internal model.
“If the behavioral response to the catch trials produces a movement that is the mirror image of the initial change in response caused by the imposed perturbation, this provides evidence that the motor system has incorporated the perturbation into its internal motor plan and thus updated its internal model of the consequences of its motor command.”
Quote in the paperSubstantial claim1 of 1 sources checked- cites [15] Berniker M, Kording K. Estimating the sources of motor errors for adaptation and generalization. Nat Neurosci. 2008;11:1454–61. source
The Results section (“Generalization to natural hand movements”; page unavailable) says that removing a force field produces aftereffects in the opposite orientation because the model has updated its estimates of body and world properties. This supports interpreting an opposite-direction response as evidence of adaptation, but the passage does not specifically discuss catch trials or establish that the resulting movement is a mirror image of the initial perturbation-induced movement. (LLM, conf=0.82)
Experimental — accuracy not yet measured
Classified as probably not a substantial claim.
PremisecitationThe brain updates its internal model of movement consequences to adapt to new circumstances.
“Studies have suggested that in order to deal with such challenges, the brain updates its internal model of the consequences of movements in order to adapt to the new circumstances [15].”
Quote in the paperSubstantial claim1 of 1 sources checked- cites [15] Berniker M, Kording K. Estimating the sources of motor errors for adaptation and generalization. Nat Neurosci. 2008;11:1454–61. source
May combine two claims.
Interpretationown dataRostral fastigial nucleus responses do not represent absolute head or body motion; instead they estimate unexpected motion needed for postural maintenance and spatial orientation.
“Thus, neuronal responses do not encode a representation of absolute head or body motion but rather provide an estimate of unexpected motion required for the maintenance of posture and accurate spatial orientation.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationThe relationship between the motor command and the resulting movement changes over time because of development, injury, or other external factors.
“In real life, the relationship between the brain's motor command and the resulting movement (and thus sensory feedback) will change over time due to, for example, development, injury or other external factors[3].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [3] Shadmehr R, Smith MA, Krakauer JW. Error correction, sensory prediction, and adaptation in motor control. Annu Rev Neurosci. 2010;33:89–108. source
May combine two claims.
InterpretationreasoningThe brain computes vestibular prediction error signals during active motion, which permits selective encoding of sensory exafference.
“Taken together, these findings suggest that the brain computes vestibular prediction error signals during active motion, thereby allowing the selective encoding of sensory exafference.”
Quote in the paperSubstantial claimMay combine two claims.
PremisecitationSingle-unit recordings in primates and imaging studies in normal humans show increased cerebellar activity when sensory feedback does not match expectation.
“However, while single-unit recording studies in primates [9] and imaging studies in normal humans have shown increased activity in the cerebellum when sensory feedback does not match what is expected [10, 11]”
Quote in the paperSubstantial claim0 of 3 sources checked- cites [9] Bauswein E, Kolb FP, Leimbeck B, Rubia FJ. Simple and complex spike activity of cerebellar Purkinje cells during active and passive movements in the awake monkey. J Physiol. 1983;339:379–94. source
- cites [10] Blakemore SJ, Frith CD, Wolpert DM. Spatio-temporal prediction modulates the perception of self-produced stimuli. J Cogn Neurosci. 1999;11:551–9. source
- cites [11] Jenmalm P, Schmitz C, Forssberg H, Ehrsson HH. Lighter or heavier than predicted: neural correlates of corrective mechanisms during erroneously programmed lifts. J Neurosci. 2006;26:9015–21. source
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationSensory prediction errors drive motor learning in humans.
“Consistent with this idea, recent behavioural studies in humans have shown sensory prediction errors drive motor learning [3].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [3] Shadmehr R, Smith MA, Krakauer JW. Error correction, sensory prediction, and adaptation in motor control. Annu Rev Neurosci. 2010;33:89–108. source
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationNeurons in lateral crus I of the rodent cerebellum respond robustly and selectively, within 10 ms, to stimulation of whisking-related sensory and motor cortical areas.
“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].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [16] Proville RD, Spolidoro M, Guyon N, Dugué GP, Selimi F, Isope P, et al. Cerebellum involvement in cortical sensorimotor circuits for the control of voluntary movements. Nat Neurosci. 2014;17(9):1233–9. source
Classified as probably not a substantial claim.
PremisecitationThe cerebellum is thought to act as a forward model that predicts the sensory consequences of self-generated movement.
“The cerebellum is generally thought to act as a forward model that predicts the sensory consequences of self-generated movement [reviewed in 2].”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [reviewed in 2]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Classified as probably not a substantial claim.
PremisecitationThe brain builds an internal model of the expected sensory consequences of movement from an efference copy of the self-produced motor command.
“It had been proposed that our brain constructs an internal model of the expected sensory consequences of movement based on an efference copy of the self-produced motor command [7].”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [7] Roy JE, Cullen KE. Dissociating self-generated from passively applied head motion: neural mechanisms in the vestibular nuclei. J Neurosci. 2004;24:2102–11. source
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationSingle-unit recordings in the fish electrosensory system show that cerebellum-like circuitry computes predictions about the sensory consequences of the animal's own behavior.
“This idea is supported by single unit recording studies in the fish electrosensory system showing that their cerebellum-like circuitry computes predictions about the sensory consequences of the animals' own behavior [8].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [8] Sawtell NB, Bell CC. Adaptive processing in electrosensory systems: links to cerebellar plasticity and learning. J Physiol Paris. 2008;102:223–32. source
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationCerebellar cortex neurons often significantly lead or lag movement during reaching or manual tracking.
“Finally, it is noteworthy that the responses of neurons in the cerebellar cortex often significantly lead or lag movement during movements such as reaching or manual tracking [reviewed in 1].”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [reviewed in 1]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
May combine two claims.
PremisecitationVestibular afferents carry reafference and exafference with comparable fidelity, but neurons at the first central stage of vestibular processing respond preferentially to exafference.
“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.”
- Also stated in: § Encoding of sensory prediction errors in the rostral fastigial nucleus · plain
“While vestibular afferents similarly encode vestibular reafference and exafference during self-motion neurons at the subsequent stage of sensory processing preferentially respond to vestibular exafference [6].”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [6] Cullen KE. The neural encoding of self-motion. Curr Opin Neurobiol. 2011;21:587–95. source
- Also stated in: § Encoding of sensory prediction errors in the rostral fastigial nucleus · plain
The paper relies on this without support.
Before this work, no neural correlate of sensory prediction error had been found.
“However, to date, a neural correlate for sensory prediction error has not yet been found.”
The paper relies on this without support.
The neural mechanisms that compute sensory exafference had remained unclear.
“Despite long-standing interest in the computations required for accurate motor control and the role of the cerebellum in these computations, the neural mechanisms underlying the computation of sensory exafference had remained unclear.”
The paper relies on this without support.
The idea that the cerebellum computes an explicit estimate of the sensory consequences of unexpected movement had not been tested.
“However, while single-unit recording studies in primates [9] and imaging studies in normal humans have shown increased activity in the cerebellum when sensory feedback does not match what is expected [10, 11], the proposal that the cerebellum computes an explicit estimate of the sensory consequences of unexpected movement had not been tested.”
The paper relies on this without support.
In everyday life, exafference and reafference are often experienced at the same time.
“Notably, in everyday life, exafference and reafference are often experienced simultaneously, making it crucial to address whether neurons encode sensory prediction errors demonstrating the anticipation and cancellation of reafferent effects under conditions in which active and passive stimulation are concurrent.”
The paper relies on this without support.
Sensory prediction errors arise from changes in the effector or world as well as from externally applied sensory stimulation.
“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.”
The paper relies on this without support.
Sensory prediction errors are generally thought to be computed in the cerebellum.
“It is generally thought that sensory prediction errors are computed in the cerebellum, yet it has been challenging to explicitly demonstrate this.”
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Highlights from the 28th Annual Meeting of the Society for the Neural Control of Movement
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Velázquez-Vargas, C. A., Daw, N. D., & Taylor, J. A. (2024) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1012471 · Cited by 9 · see citing works
Neurophysiological Evidence of Sensory Prediction Errors Driving Speech Sensorimotor Adaptation
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The social dimension of peripersonal space
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Özyurt, M. G., Chiasson, S., Laliberté, A. M., Nascimento, F., KHAN, E. S. I., Mayer, W. P., Bhumbra, G. S., Akay, T., Bui, T. V., Beato, M., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.08.27.672590 · Cited by 4 · see citing works
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- Authors
- Cullen, K. E., & Brooks, J. X.
- Affiliations
- McGill University (CA)
- Corresponding author
- Cullen, Kathleen E.
- ORCID
- Cullen, Kathleen E.
- Venue
- The Cerebellum
- Published
- 2014-10-08
- Volume
- 14
- Issue
- 1
- Pages
- 31-34
- ISSN
- 1473-4222 (ISSN-L)
- 1473-4230
- PMC
- PMC4320652
- OpenAlex
- W2063309468
- Cited by
- 60
- References
- 17
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 6 · 2023: 5 · 2022: 2 · 2021: 5 · 2020: 8 · 2019: 5 · 2018: 5 · 2017: 10 · 2016: 3 · 2015: 2
- FWCI
- 2.81
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- The Cerebellum (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Neurology › Vestibular and auditory disorders
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Keywords
- sensory prediction error, internal models, deep cerebellar nuclei, self-motion perception, motor control, monkeys
- MeSH terms
- Animals, Haplorhini, Cerebellum, Feedback, Perception, Psychomotor Performance
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.
Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-09-28.
Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-09-28.
Cited sources are checked by gpt-6-sol.
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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