A Pathway in Primate Brain for Internal Monitoring of Movements
Open accessAbstract
It is essential to keep track of the movements we make, and one way to do that is to monitor correlates, or corollary discharges, of neuronal movement commands. We hypothesized that a previously identified pathway from brainstem to frontal cortex might carry corollary discharge signals. We found that neuronal activity in this pathway encodes upcoming eye movements and that inactivating the pathway impairs sequential eye movements consistent with loss of corollary discharge without affecting single eye movements. These results identify a pathway in the brain of the primate Macaca mulatta that conveys corollary discharge signals.
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Animal and patient investigations have supplied the strongest direct support for forward models.
“Most direct evidence for forward models has been obtained in animal preparations (e.g., Troyer and Doupe, 2000; Sommer and Wurtz, 2002) or patient studies (e.g., Desmurget et al., 2009).”
From Mental imagery of speech and movement implicates the dynamics of internal forward models (2010) · cites this paper as Sommer and Wurtz, 2002
Electrophysiological recordings from a transiently inactivated circuit in the brain have shed light on how corollary discharge is used for saccadic sequencing in rhesus monkeys.
“Electrophysiological recordings from a transiently inactivated circuit in the brain have shed some light on how CD is used for saccadic sequencing in rhesus monkeys62,63,65 (FIG. 6Aa).”
From Corollary discharge across the animal kingdom (2008) · cites this paper as [62]
The results conformed to the prediction that impairing corollary discharge of the first eye movements would cause incorrect second saccades, revealing a loss of corollary discharge.
“The results conformed to this prediction, revealing a loss of CD.”
From Corollary discharge across the animal kingdom (2008) · cites this paper as [62]
Corollary discharge has repeatedly been implicated in the process of updating the internal record of the current saccade to facilitate planning the next.
“CD has repeatedly been implicated in this process59–64.”
From Corollary discharge across the animal kingdom (2008) · cites this paper as [62]
When the midbrain-to-prefrontal pathway was inactivated by muscimol, behavioural deficits in the simplest saccadic sequencing task were observed.
“When this pathway was inactivated by muscimol, a GABAA (γ-aminobutyric acid receptor type A) agonist, behavioural deficits in the simplest saccadic sequencing task were observed.”
From Corollary discharge across the animal kingdom (2008) · cites this paper as [62]
Neurons that connect the midbrain to the prefrontal cortex transmit bursts of action potentials that encode saccadic parameters.
“Neurons that connect the midbrain to the prefrontal cortex transmit bursts of action potentials that encode saccadic parameters.”
From Corollary discharge across the animal kingdom (2008) · cites this paper as [62]
In this saccadic sequencing example, corollary discharge emerges from a lower-level motor structure and ascends the neuraxis to impinge on a higher-level executive centre.
“This is an example in which CD emerges from a lower-level motor structure and ascends the neuraxis to impinge on a higher-level executive centre (FIG. 6Ab).”
From Corollary discharge across the animal kingdom (2008) · cites this paper as [62]
In the visuosaccadic system of the primate, a corollary discharge circuit has a role in sensorimotor planning as well as in sensory stability.
“One example we reviewed was from the visuosaccadic system of the primate40,62. In this system, a CD circuit has a role in sensorimotor planning as well as in sensory stability (compare FIG. 6A with BOX 2).”
From Corollary discharge across the animal kingdom (2008) · cites this paper as [62]
Cites
Optimal feedback control as a theory of motor coordination
Todorov, E., & Jordan, M. I. (2002) · Nature Neuroscience · doi:10.1038/nn963 · Cited by 3,081 · see citing works
The updating of the representation of visual space in parietal cortex by intended eye movements
Duhamel, J.-R., Colby, C. L., & Goldberg, M. E. (1992) · Science · doi:10.1126/science.1553535 · Cited by 1,966 · see citing works
Neural basis of the spontaneous optokinetic response produced by visual inversion
Sperry, R. W. (1950) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0055479 · Cited by 1,789 · see citing works
Wolpert, D. M., & Flanagan, J. R. (2001) · Current Biology · doi:10.1016/s0960-9822(01)00432-8 · Cited by 1,257 · see citing works
An analysis of the saccadic system by means of double step stimuli
Becker, W., & Jürgens, R. (1979) · Vision Research · doi:10.1016/0042-6989(79)90222-0 · Cited by 953 · see citing works
Changes in visual perception at the time of saccades
Ross, J., Morrone, M. C., Goldberg, M. E., & Burr, D. C. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01685-4 · Cited by 631 · see citing works
Dissociation of visual and saccade-related responses in superior colliculus neurons
Mays, L. E., & Sparks, D. L. (1980) · Journal of Neurophysiology · doi:10.1152/jn.1980.43.1.207 · Cited by 556 · see citing works
Corollary Discharge Provides Accurate Eye Position Information to the Oculomotor System
Guthrie, B. L., Porter, J. D., & Sparks, D. L. (1983) · Science · doi:10.1126/science.6612334 · Cited by 476 · see citing works
Spatial Processing in the Monkey Frontal Eye Field. I. Predictive Visual Responses
Umeno, M. M., & Goldberg, M. E. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.78.3.1373 · Cited by 462 · see citing works
Multivariate Statistics: A Practical Approach
Hawkins, D. M., Flury, B. N., & Riedwyl, H. (1990) · Technometrics · doi:10.2307/1269856 · Cited by 417 · see citing works
Lynch, J. C., Hoover, J. E., & Strick, P. L. (1994) · Experimental Brain Research · doi:10.1007/bf00227293 · Cited by 306 · see citing works
Proprioceptive knowledge of eye position
Steinbach, M. J. (1987) · Vision Research · doi:10.1016/0042-6989(87)90103-9 · Cited by 301 · see citing works
Eye Movements Modulate Visual Receptive Fields of V4 Neurons
Tolias, A. S., Moore, T., Smirnakis, S. M., Tehovnik, E. J., Siapas, A. G., & Schiller, P. H. (2001) · Neuron · doi:10.1016/s0896-6273(01)00250-1 · Cited by 295 · see citing works
Sensorimotor transformation during eye movements to remembered visual targets
Gnadt, J., Bracewell, R. M., & Andersen, R. A. (1991) · Vision Research · doi:10.1016/0042-6989(91)90010-3 · Cited by 233 · see citing works
Cortical control of double‐step saccades: Implications for spatial orientation
Heide, W., Blankenburg, M. R., Zimmermann, E., & Kömpf, D. (1995) · Annals of Neurology · doi:10.1002/ana.410380508 · Cited by 217 · see citing works
Lomber, S. G. (1999) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(98)00160-5 · Cited by 206 · see citing works
SACCADIC DYSMETRIA IN A PATIENT WITH A RIGHT FRONTOPARIETAL LESION
Duhamel, J., Goldberg, M. E., FitzGibbon, E. J., Angela Sirigu, B., & Grafman, J. H. (1992) · Brain · doi:10.1093/brain/115.5.1387 · Cited by 204 · see citing works
The functions of the proprioceptors of the eye muscles
Donaldson, I. M. L. (2000) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2000.0732 · Cited by 185 · see citing works
Troyer, T. W., & Doupe, A. J. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.84.3.1204 · Cited by 145 · see citing works
A review of the role of efference copy in sensory and oculomotor control systems
Bridgeman, B. (1995) · Annals of Biomedical Engineering · doi:10.1007/bf02584441 · Cited by 126 · see citing works
Oculomotor function in the rhesus monkey after deafferentation of the extraocular muscles
Lewis, R. F., Zee, D. S., Hayman, M., & Tamargo, R. J. (2001) · Experimental Brain Research · doi:10.1007/s002210100876 · Cited by 99 · see citing works
Impairment of extraretinal eye position signals after central thalamic lesions in humans
Gaymard, B. M., Rivaud-Péchoux, S., & Pierrot‐Deseilligny, C. (1994) · Experimental Brain Research · doi:10.1007/bf00232433 · Cited by 61 · see citing works
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Error Correction, Sensory Prediction, and Adaptation in Motor Control
Shadmehr, R., Smith, M. A., & Krakauer, J. W. (2010) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-060909-153135 · Cited by 1,869 · see citing works
Corollary discharge across the animal kingdom
Crapse, T. B., & Sommer, M. A. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2457 · Cited by 789 · see citing works
Self-citationA synaptic and circuit basis for corollary discharge in the auditory cortex
Schneider, D. M., Nelson, A., & Mooney, R. (2014) · Nature · doi:10.1038/nature13724 · Cited by 580 · see citing works
Histed, M. H., Bonin, V., & Reid, R. C. (2009) · Neuron · doi:10.1016/j.neuron.2009.07.016 · Cited by 604 · see citing works
Influence of the thalamus on spatial visual processing in frontal cortex
Sommer, M. A., & Wurtz, R. H. (2006) · Nature · doi:10.1038/nature05279 · Cited by 520 · see citing works
Self-citationBrain Circuits for the Internal Monitoring of Movements
Sommer, M. A., & Wurtz, R. H. (2008) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.31.060407.125627 · Cited by 508 · see citing works
Self-citationMitchell, A. S. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.03.001 · Cited by 323 · see citing works
Selective D2 receptor actions on the functional circuitry of working memory
Wang, M., Vijayraghavan, S., & Goldman-Rakic, P. S. (2004) · Science · doi:10.1126/science.1091162 · Cited by 319 · see citing works
Mental imagery of speech and movement implicates the dynamics of internal forward models
Tian, X. (2010) · Frontiers in Psychology · doi:10.3389/fpsyg.2010.00166 · Cited by 259 · see citing works
“Most direct evidence for forward models has been obtained in animal preparations (e.g., Troyer and Doupe, 2000; Sommer and Wurtz, 2002) or patient studies (e.”
Sommer, M. A., & Wurtz, R. H. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00740.2003 · Cited by 254 · see citing works
Self-citationPeters (2010) · doi:10.1016/j.neuron.2010.03.027 · Cited by 244 · see citing works
A circuit for motor cortical modulation of auditory cortical activity
Nelson, A., Schneider, D. M., Takatoh, J., Sakurai, K., Wang, F., & Mooney, R. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.2275-13.2013 · Cited by 213 · see citing works
The Cellular Basis of a Corollary Discharge
Poulet, J. F. A., & Hedwig, B. (2006) · Science · doi:10.1126/science.1120847 · Cited by 234 · see citing works
Cellular evidence for efference copy in Drosophila visuomotor processing
Kim, A. J., Fitzgerald, J. K., & Maimon, G. (2015) · Nature Neuroscience · doi:10.1038/nn.4083 · Cited by 187 · see citing works
Neuronal Basis for Object Location in the Vibrissa Scanning Sensorimotor System
Kleinfeld, D., & Deschênes, M. (2011) · Neuron · doi:10.1016/j.neuron.2011.10.009 · Cited by 153 · see citing works
Dynamics of Auditory–Vocal Interaction in Monkey Auditory Cortex
Eliades, S. J., & Wang, X. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhi030 · Cited by 150 · see citing works
Ouhaz, Z., Fleming, H., & Mitchell, A. S. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00033 · Cited by 142 · see citing works
Thalamic pathways for active vision
Wurtz, R. H., McAlonan, K., Cavanaugh, J., & Berman, R. A. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2011.02.004 · Cited by 127 · see citing works
Self-citationThe thalamus as a monitor of motor outputs.
Guillery, R. W., & Sherman, S. M. (2002) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2002.1171 · Cited by 128 · see citing works
The yin and yang of sleep and attention
Kirszenblat, L., & van Swinderen, B. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.10.001 · Cited by 81 · see citing works
Untangling Brain-Wide Dynamics in Consciousness by Cross-Embedding
Tajima, S., Yanagawa, T., Fujii, N., & Toyoizumi, T. (2015) · PLOS Computational Biology · doi:10.1371/journal.pcbi.1004537 · Cited by 76 · see citing works
Oculomotor prediction: A window into the psychotic mind
Thakkar, K. N., Diwadkar, V. A., & Rolfs, M. (2017) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2017.02.001 · Cited by 66 · see citing works
Inactivation of the central thalamus delays self-timed saccades
Tanaka, M. (2006) · Nature Neuroscience · doi:10.1038/nn1617 · Cited by 54 · see citing works
Altered processing of corollary discharge in thalamic lesion patients
Bellebaum, C., Hoffmann, K., Koch, B., Schwarz, M., & Daum, I. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05114.x · Cited by 35 · see citing works
Rösler, L., Rolfs, M., van der Stigchel, S., Neggers, S. F. W., Cahn, W., Kahn, R. S., & Thakkar, K. N. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00155.2015 · Cited by 34 · see citing works
- Authors
- Sommer, M. A., & Wurtz, R. H.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Sommer, Marc A.
- ORCID
- Sommer, Marc A.
- Venue
- Science
- Published
- 2002-05-24
- Volume
- 296
- Issue
- 5572
- Pages
- 1480-1482
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2122905397
- Cited by
- 565
- References
- 22
- Citations by year
- 2026: 9 · 2025: 18 · 2024: 19 · 2023: 22 · 2022: 18 · 2021: 23 · 2020: 20 · 2019: 25 · 2018: 23 · 2017: 22 · 2016: 25 · 2015: 33 · 2014: 25 · 2013: 23 · 2012: 34
- FWCI
- 10.39
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Licence
- cc-by-nc-nd
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- DukeSpace (Duke University) (submittedVersion, cc-by-nc-nd)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- corollary discharge, motion monitoring, eye movements, brainstem, frontal cortex, neuronal activity, rhesus monkeys
- MeSH terms
- Animals, Brain Mapping, Fixation, Ocular, Frontal Lobe, Macaca mulatta, Muscimol, Neural Pathways, Neurons, Proprioception, Saccades, Superior Colliculi, GABA Agonists, Mediodorsal Thalamic Nucleus
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