Influence of the thalamus on spatial visual processing in frontal cortex
Open accessAbstract
Each of our movements activates our own sensory receptors, and therefore keeping track of self-movement is a necessary part of analysing sensory input. One way in which the brain keeps track of self-movement is by monitoring an internal copy, or corollary discharge, of motor commands. This concept could explain why we perceive a stable visual world despite our frequent quick, or saccadic, eye movements: corollary discharge about each saccade would permit the visual system to ignore saccade-induced visual changes. The critical missing link has been the connection between corollary discharge and visual processing. Here we show that such a link is formed by a corollary discharge from the thalamus that targets the frontal cortex. In the thalamus, neurons in the mediodorsal nucleus relay a corollary discharge of saccades from the midbrain superior colliculus to the cortical frontal eye field. In the frontal eye field, neurons use corollary discharge to shift their visual receptive fields spatially before saccades. We tested the hypothesis that these two components-a pathway for corollary discharge and neurons with shifting receptive fields-form a circuit in which the corollary discharge drives the shift. First we showed that the known spatial and temporal properties of the corollary discharge predict the dynamic changes in spatial visual processing of cortical neurons when saccades are made. Then we moved from this correlation to causation by isolating single cortical neurons and showing that their spatial visual processing is impaired when corollary discharge from the thalamus is interrupted. Thus the visual processing of frontal neurons is spatiotemporally matched with, and functionally dependent on, corollary discharge input from the thalamus. These experiments establish the first link between corollary discharge and visual processing, delineate a brain circuit that is well suited for mediating visual stability, and provide a framework for studying corollary discharge in other sensory systems.
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At least some of the CD for shifting receptive fields arises from a pathway that ascends from the midbrain to the frontal eye field.
“At least some of this CD arises from a pathway that ascends from the midbrain40,41 to the frontal eye field, a cortical structure that is involved in visual processing and eye-movement control42.”
From Corollary discharge across the animal kingdom (2008) · cites this paper as [40]
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 [40]
To date, only a few large-scale circuit-level investigations of corollary discharge that combined behaviour with physiology have been performed.
“To date, only a few large-scale circuit-level investigations of CD that combined behaviour with physiology have been performed38,40.”
From Corollary discharge across the animal kingdom (2008) · cites this paper as [40]
Cites
Das Reafferenzprinzip: Wechselwirkungen zwischen Zentralnervensystem und Peripherie
von Holst, E., & Mittelstaedt, H. (1950) · Naturwissenschaften · doi:10.1007/bf00622503 · Cited by 2,655 · 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
(1964) · McGraw-Hill eBooks · Cited by 838 · see citing works
Helmholtz's treatise on physiological optics
Southall, J. P. C. (1924) · Journal of the Franklin Institute · doi:10.1016/s0016-0032(24)90484-4 · Cited by 701 · see citing works
The neurobiology of saccadic eye movements.
Wurtz, R. H., & Goldberg, M. E. (1989) · PubMed · Cited by 630 · see citing works
Self-citationA Pathway in Primate Brain for Internal Monitoring of Movements
Sommer, M. A., & Wurtz, R. H. (2002) · Science · doi:10.1126/science.1069590 · Cited by 565 · see citing works
Self-citationCorollary 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
The Frontal Granular Cortex and Behavior.
Cole, M. (1964) · Archives of Neurology · doi:10.1001/archneur.1964.00460240114017 · Cited by 467 · 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
Updating of the visual representation in monkey striate and extrastriate cortex during saccades
Nakamura, K., & Colby, C. L. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.052379899 · Cited by 438 · see citing works
Sommer, M. A., & Wurtz, R. H. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.4.1979 · Cited by 350 · see citing works
Self-citationSommer, M. A., & Wurtz, R. H. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00738.2003 · Cited by 339 · see citing works
Self-citationLynch, J. C., Hoover, J. E., & Strick, P. L. (1994) · Experimental Brain Research · doi:10.1007/bf00227293 · Cited by 306 · see citing works
Comparative Physiology of Sensory Systems
Land, M. F. (1985) · Trends in Neurosciences · doi:10.1016/0166-2236(85)90133-x · Cited by 275 · see citing works
Sommer, M. A., & Wurtz, R. H. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00740.2003 · Cited by 254 · see citing works
Self-citationKusunoki, M., & Goldberg, M. E. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00519.2002 · Cited by 211 · see citing works
Countermanding saccades in macaque
Hanes, D. P., & Schall, J. D. (1995) · Visual Neuroscience · doi:10.1017/s0952523800009482 · Cited by 208 · 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
Spatial Processing in the Monkey Frontal Eye Field
Umeno, M. M. (1997) · Medical Entomology and Zoology · Cited by 186 · see citing works
A corollary discharge maintains auditory sensitivity during sound production
Poulet, J. F. A., & Hedwig, B. (2002) · Nature · doi:10.1038/nature00919 · Cited by 160 · see citing works
Spatial Processing in the Monkey Frontal Eye Field. II. Memory Responses
Umeno, M. M., & Goldberg, M. E. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.86.5.2344 · Cited by 148 · see citing works
Identifying corollary discharges for movement in the primate brain
Wurtz, R. H., & Sommer, M. A. (2004) · Progress in brain research · doi:10.1016/s0079-6123(03)14403-2 · Cited by 106 · see citing works
Self-citationHelmholtz's Treatise on Physiological Optics
Peddie, D. W. (1926) · Nature · doi:10.1038/118074a0 · Cited by 94 · see citing works
The Neurobiology of Saccadic Eye Movements (Reviews of Oculomotor Research Vol. 3)
Donaldson, I. M. L. (1990) · Trends in Neurosciences · doi:10.1016/0166-2236(90)90154-3 · Cited by 74 · see citing works
Corollary discharge to cockroach giant interneurones
DELCOMYN, F. (1977) · Nature · doi:10.1038/269160a0 · Cited by 59 · see citing works
Cortical Substrates of Perceptual Stability during Eye Movements
Thier, P., Haarmeier, T., Chakraborty, S., Lindner, A., & Tikhonov, A. (2001) · NeuroImage · doi:10.1006/nimg.2001.0840 · Cited by 29 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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
Top-down influences on visual processing
Gilbert, C. D., & Li, W. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3476 · Cited by 1,224 · 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-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-citationNeural mechanisms of selective visual attention.
Moore, T., & Zirnsak, M. (2017) · Annual Review of Psychology · doi:10.1146/annurev-psych-122414-033400 · Cited by 471 · see citing works
Distinct functions for direct and transthalamic corticocortical connections
Sherman, S. M., & Guillery, R. W. (2011) · Journal of Neurophysiology · doi:10.1152/jn.00429.2011 · Cited by 336 · see citing works
Mitchell, A. S. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.03.001 · Cited by 323 · 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
“…in neuroscience, including in motor control (for reviews see Miall and Wolpert, 1996; Kawato, 1999; Wolpert and Ghahramani, 2000), perception (e.g., Sommer and Wurtz, 2006; for review see Sommer and Wurtz, 2008), and different aspects of cognition (for reviews see Blakemore and Decety, 2001;…”
Gee, S., Ellwood, I., Patel, T., Luongo, F., Deisseroth, K., & Sohal, V. S. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.5835-11.2012 · Cited by 214 · see citing works
Buzsáki, G., & Llinás, R. (2017) · Science · doi:10.1126/science.aan8869 · Cited by 175 · see citing works
Zheng, Z. Z., Munhall, K. G., & Johnsrude, I. S. (2010) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21324 · Cited by 177 · see citing works
Quantitative Predictions Orchestrate Visual Signaling in Drosophila
Kim, A. J., Fenk, L. M., Lyu, C., & Maimon, G. (2017) · Cell · doi:10.1016/j.cell.2016.12.005 · Cited by 139 · 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-citationGrossberg, S. (2017) · Neural Networks · doi:10.1016/j.neunet.2016.11.003 · Cited by 120 · see citing works
Anticipating the future: Automatic prediction failures in schizophrenia
Ford, J. M., & Mathalon, D. H. (2012) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2011.09.004 · Cited by 113 · see citing works
Thalamic contributions to the state and contents of consciousness
Whyte, C. J., Redinbaugh, M. J., Shine, J. M., & Saalmann, Y. B. (2024) · Neuron · doi:10.1016/j.neuron.2024.04.019 · Cited by 105 · 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
Corollary Discharge Dysfunction in Schizophrenia: Evidence for an Elemental Deficit
Mathalon, D. H., & Ford, J. M. (2008) · Clinical EEG and Neuroscience · doi:10.1177/155005940803900212 · Cited by 60 · see citing works
Vijayraghavan, S., Major, A. J., & Everling, S. (2018) · Neuron · doi:10.1016/j.neuron.2018.05.027 · Cited by 51 · see citing works
Corollary discharge circuits for saccadic modulation of the pigeon visual system
Yang, Y., Cao, P., Yang, Y., & Wang, S.-R. (2008) · Nature Neuroscience · doi:10.1038/nn.2107 · Cited by 41 · see citing works
Paraskevoudi, N., & Pezaris, J. S. (2019) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2018.00073 · Cited by 39 · see citing works
Retinotopic to spatiotopic mapping in blind patients implanted with the Argus II retinal prosthesis
Caspi, A., Roy, A., Dorn, J. D., & Greenberg, R. J. (2017) · Investigative Opthalmology & Visual Science · doi:10.1167/iovs.16-20398 · Cited by 32 · see citing works
Thalamic oscillations distinguish natural states of consciousness in humans
Chowdhury, A., Wu, X., Beilner, T., Schreiner, T., Koeglsperger, T., Mehrkens, J.-H., Remi, J., Vollmar, C., Kaufmann, E., & Staudigl, T. (2026) · Nature Human Behaviour · doi:10.1038/s41562-026-02446-z · Cited by 1 · 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
- Nature
- Published
- 2006-11
- Volume
- 444
- Issue
- 7117
- Pages
- 374-377
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2065943687
- Cited by
- 520
- References
- 27
- Citations by year
- 2026: 13 · 2025: 18 · 2024: 18 · 2023: 27 · 2022: 14 · 2021: 23 · 2020: 28 · 2019: 38 · 2018: 26 · 2017: 24 · 2016: 28 · 2015: 30 · 2014: 30 · 2013: 25 · 2012: 38
- FWCI
- 12.94
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Licence
- cc-by-nc-nd
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- DukeSpace (Duke University) (submittedVersion, cc-by-nc-nd)
- Funders
- National Institutes of Health
- National Eye Institute
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- corollary discharge, saccades, thalamus, mediodorsal thalamus, frontal eye field, perceptual stability, superior colliculus, single-unit recording
- MeSH terms
- Animals, Frontal Lobe, Macaca mulatta, Neurons, Thalamus, Visual Perception
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