Optogenetic inactivation modifies monkey visuomotor behavior
Open accessAbstract
A critical technique for understanding how neuronal activity contributes to behavior is determining whether perturbing it changes behavior. The advent of optogenetic techniques allows the immediately reversible alteration of neuronal activity in contrast to chemical approaches lasting minutes to hours. Modification of behavior using optogenetics has had substantial success in rodents but has not been as successful in monkeys. Here, we show how optogenetic inactivation of superior colliculus neurons in awake monkeys leads to clear and repeatable behavioral deficits in the metrics of saccadic eye movements. We used our observations to evaluate principles governing the use of optogenetic techniques in the study of the neuronal bases of behavior in monkeys, particularly how experimental design must address relevant parameters, such as the application of light to subcortical structures, the spread of viral injections, and the extent of neuronal inactivation with light.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
So far, optogenetics has had little success in altering behavior in non-human primates.
“Although minimal success has been achieved to date, several groups are currently investing significant resources in using optogenetics to generate behavioral changes in non-human primates 138–143.”
From DISSECTING OCD CIRCUITS: FROM ANIMAL MODELS TO TARGETED TREATMENTS: Review: Dissecting OCD Circuits: Animals to Treatments (2015) · cites this paper as [142]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Eye movements evoked by collicular stimulation in the alert monkey
Robinson, D. A. (1972) · Vision Research · doi:10.1016/0042-6989(72)90070-3 · Cited by 1,350 · see citing works
High-performance genetically targetable optical neural silencing by light-driven proton pumps
Chow, B. Y., Han, X., Dobry, A. S., Qian, X., Chuong, A. S., Li, M., Henninger, M. A., Belfort, G. M., Lin, Y., Monahan, P. E., et al. (2010) · Nature · doi:10.1038/nature08652 · Cited by 1,188 · see citing works
Self-citationOptogenetic investigation of neural circuits underlying brain disease in animal models
Tye, K. M., & Deisseroth, K. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3171 · Cited by 745 · see citing works
Population coding of saccadic eye movements by neurons in the superior colliculus
Lee, C., Rohrer, W. H., & Sparks, D. L. (1988) · Nature · doi:10.1038/332357a0 · Cited by 740 · see citing works
Hikosaka, O., & Wurtz, R. H. (1985) · Journal of Neurophysiology · doi:10.1152/jn.1985.53.1.266 · Cited by 691 · see citing works
Self-citationUnix-based multiple-process system, for real-time data acquisition and control
Hays, A. V., Richmond, B. J., & Optican, L. M. (1982) · OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) · Cited by 497 · see citing works
Millisecond-Timescale Optical Control of Neural Dynamics in the Nonhuman Primate Brain
Han, X., Qian, X., Bernstein, J. G., Zhou, H., Franzesi, G. T., Stern, P., Bronson, R. T., Graybiel, A. M., Desimone, R., & Boyden, E. S. (2009) · Neuron · doi:10.1016/j.neuron.2009.03.011 · Cited by 497 · see citing works
Self-citationHan, X., Chow, B. Y., Zhou, H., Klapoetke, N. C., Chuong, A. S., Rajimehr, R., Yang, A., Baratta, M. V., Winkle, J. A., Desimone, R., et al. (2011) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2011.00018 · Cited by 490 · see citing works
Self-citationAn optogenetic toolbox designed for primates
Diester, I., Kaufman, M. T., Mogri, M., Pashaie, R., Goo, W., Yizhar, O., Ramakrishnan, C., Deisseroth, K., & Shenoy, K. V. (2011) · Nature Neuroscience · doi:10.1038/nn.2749 · Cited by 443 · see citing works
Cavanaugh, J. R., Bair, W., & Movshon, J. A. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00693.2001 · Cited by 426 · see citing works
Self-citationSommer, M. A., & Wurtz, R. H. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.4.1979 · Cited by 350 · see citing works
Self-citationLeventhal, A. G., Thompson, K. G., Liu, D., Zhou, Y., & Ault, S. J. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-03-01808.1995 · Cited by 306 · see citing works
Saccade-related activity in monkey superior colliculus. II. Spread of activity during saccades
Munoz, D. P., & Wurtz, R. H. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.73.6.2334 · Cited by 299 · see citing works
Self-citationA grid system and a microsyringe for single cell recording
Crist, C. F., Yamasaki, D. S. G., Komatsu, H., & Wurtz, R. H. (1988) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(88)90160-4 · Cited by 277 · see citing works
Self-citationSaccadic eye movements following injection of lidocaine into the superior colliculus
Hikosaka, O., & Wurtz, R. H. (1986) · Experimental Brain Research · doi:10.1007/bf00237578 · Cited by 238 · see citing works
Self-citationNakahara, H., Morita, K., Wurtz, R. H., & Optican, L. M. (2006) · Journal of Neurophysiology · doi:10.1152/jn.01372.2005 · Cited by 23 · see citing works
Self-citationKnöpfel, T., & Boyden, E. S. (2012) · Progress in brain research · doi:10.1016/b978-0-444-59426-6.00019-7 · Cited by 6 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 1
- Knopfel T Boyden ES Tools for observing and controlling specific molecular or physiological pathways in intact cells and tissues. Preface Prog Brain Res 2012 196 vii viii 22341330
Cited by
Sorted by citations
Optogenetic dissection of medial prefrontal cortex circuitry
Riga, D., Matos, M. R., Glas, A., Smit, A. B., Spijker, S., & Van den Oever, M. C. (2014) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2014.00230 · Cited by 208 · see citing works
Borton, D., Micera, S., Millán, J. D. R., & Courtine, G. (2013) · Science Translational Medicine · doi:10.1126/scitranslmed.3005968 · Cited by 171 · see citing works
Beyond the brain: Optogenetic control in the spinal cord and peripheral nervous system
Montgomery, K. L., Iyer, S. M., Christensen, A. J., Deisseroth, K., & Delp, S. L. (2016) · Science Translational Medicine · doi:10.1126/scitranslmed.aad7577 · Cited by 147 · see citing works
Optogenetics through windows on the brain in the nonhuman primate
Ruiz, O., Lustig, B. R., Nassi, J. J., Cetin, A., Reynolds, J. H., Albright, T. D., Callaway, E. M., Stoner, G. R., & Roe, A. W. (2013) · Journal of Neurophysiology · doi:10.1152/jn.00153.2013 · Cited by 132 · see citing works
Ahmari, S. E., & Dougherty, D. D. (2015) · Depression and Anxiety · doi:10.1002/da.22367 · Cited by 128 · see citing works
A coaxial optrode as multifunction write-read probe for optogenetic studies in non-human primates
Ozden, I., Wang, J., Lu, Y., May, T., Lee, J., Goo, W., O'Shea, D. J., Kalanithi, P., Diester, I., Diagne, M., et al. (2013) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2013.06.011 · Cited by 97 · see citing works
Optogenetic and electrical microstimulation systematically bias visuospatial choice in primates
Dai, J., Brooks, D. I., & Sheinberg, D. L. (2014) · Current Biology · doi:10.1016/j.cub.2013.11.011 · Cited by 97 · see citing works
Synaptic gradients transform object location to action
Dombrovski, M., Peek, M. Y., Park, J.-Y., Vaccari, A., Sumathipala, M., Morrow, C., Breads, P., Zhao, A., Kurmangaliyev, Y. Z., Sanfilippo, P., et al. (2023) · Nature · doi:10.1038/s41586-022-05562-8 · Cited by 67 · see citing works
- Authors
- Cavanaugh, J., Monosov, I. E., McAlonan, K., Berman, R., Smith, M. K., Cao, V., Wang, K. H., Boyden, E. S., & Wurtz, R. H.
- Affiliations
- National Institutes of Health (US)
- Massachusetts Institute of Technology (US)
- Corresponding author
- Cavanaugh, James
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2012-12
- Volume
- 76
- Issue
- 5
- Pages
- 901-907
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC4311889
- OpenAlex
- W2054041034
- Cited by
- 124
- References
- 17
- Citations by year
- 2026: 4 · 2025: 3 · 2024: 1 · 2023: 6 · 2022: 4 · 2021: 6 · 2020: 12 · 2019: 9 · 2018: 6 · 2017: 19 · 2016: 17 · 2015: 15 · 2014: 8 · 2013: 14
- FWCI
- 4.88
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-nd)
- Funders
- National Institutes of Health
- National Eye Institute (ZIAEY000109)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Photoreceptor and optogenetics research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- optogenetic inactivation, superior colliculus, saccades, visuomotor behavior, monkeys, behavioral deficits
- MeSH terms
- Dependovirus, Animals, Brain Mapping, Cell Count, Lasers, Macaca mulatta, Male, Neurons, Orientation, Phosphopyruvate Hydratase, Photic Stimulation, Reaction Time, Saccades, Superior Colliculi, Green Fluorescent Proteins, Optogenetics
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 ›
Are you an author, or do you see a problem with this page? Request a review
