Location of saccade-related neurons in the macaque superior colliculus
Abstract
The locations of saccade-related neurons were studied in the superior colliculi of two adult rhesus monkeys (Macaca mulatta) by placing marking lesions at the sites of physiologically characterized cells and comparing these histologically identified sites with the collicular laminae and acetylcholinesterase (AChE)-rich patches. Three major conclusions were drawn on the basis of 39 histologically identified sites at which saccade-related neurons were recorded. First, saccade-related neurons were distributed from the ventral half of the optic layer through the deep gray layer, and were most concentrated in the intermediate gray and white layers. Second, there was a clear relationship between the discharge characteristics of these saccade-related neurons and the depths at which they were found. Neurons having presaccadic bursts, defined as clipped and partially-clipped, tended to be encountered more dorsally, and neurons that did not have bursts (unclipped) were encountered more ventrally. Although cells having different discharge characteristics seemed to be organized along a dorsoventral axis, there was no compelling evidence that these properties were specified by their laminar locations. Third, there was no clear correlation between the locations of saccade-related neurons and the distribution of individual AChE-rich patches. Saccade-related cells were found both in the caudal superior colliculus where patches were located and in the rostral superior colliculus where patches were not found; both within and between the two tiers of AChE-rich patches in the caudal superior colliculus; and both within and between individual AChE-rich patches. However, the depth-level at which saccade-related neurons occurred generally matched the region bounded by the two tiers of AChE-rich patches in the intermediate and deep layers, and the dorsal and ventral extent of saccade-related neurons was the same as that of the AChE-rich patches.
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The superior colliculus (SC) has an important role in controlling eye movements and shifting gaze direction.
“the SC has an important role in controlling eye movements and shifting gaze direction42–44.”
From Effect of age and autism spectrum disorder on oxytocin receptor density in the human basal forebrain and midbrain (2018) · cites this paper as [43]
Cholinergic input from the pedunculopontine tegmental nucleus strongly innervates the macaque superior colliculus, and its neurones are active during saccade tasks and directly stimulate superior colliculus neurones to facilitate saccadic initiation.
“Furthermore, cholinergic input from the PPT strongly innervates the macaque SC (53), and neurones in the PPT have also been shown to be active in monkeys during saccade tasks (54) and to directly stimulate SC neurones and facilitate the initiation of saccadic eye movements (55).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [53]
Cites
A Method of Measuring Eye Movemnent Using a Scieral Search Coil in a Magnetic Field
Robinson, D. A. (1963) · IEEE Transactions on Bio-medical Electronics · doi:10.1109/tbmel.1963.4322822 · Cited by 2,214 · see citing works
Wong‐Riley, M. T. T. (1979) · Brain Research · doi:10.1016/0006-8993(79)90728-5 · Cited by 1,853 · see citing works
A method of measuring eye movements using a scleral search coil in a magnetic field
Robinson, D. A. (1963) · Medical Entomology and Zoology · Cited by 1,709 · see citing works
Implantation of magnetic search coils for measurement of eye position: An improved method
Judge, S. J., Richmond, B. J., & Chu, F. C. (1980) · Vision Research · doi:10.1016/0042-6989(80)90128-5 · Cited by 1,545 · see citing works
Silver Staining of Myelin by Means of Physical Development
Gallyas, F. (1979) · Neurological Research · doi:10.1080/01616412.1979.11739553 · Cited by 936 · see citing works
Visual-Motor Function of the Primate Superior Colliculus
Wurtz, R. H., & Albano, J. E. (1980) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.03.030180.001201 · Cited by 904 · see citing works
Self-citationSparks, D. L. (1986) · Physiological Reviews · doi:10.1152/physrev.1986.66.1.118 · Cited by 824 · see citing works
Activity of superior colliculus in behaving monkey. 3. Cells discharging before eye movements.
Wurtz, R., & Goldberg, M. E. (1972) · Journal of Neurophysiology · doi:10.1152/jn.1972.35.4.575 · Cited by 669 · see citing works
Self-citationDistribution of acetyl cholinesterase in the hippocampal region of the guinea pig
Geneser-Jensen, F. A., & Blackstad, T. W. (1971) · Cell and Tissue Research · doi:10.1007/bf00325634 · Cited by 618 · see citing works
The Mammalian Superior Colliculus: Studies of Its Morphology and Connections
Huerta, M. F., & Harting, J. K. (1984) · Springer eBooks · doi:10.1007/978-1-4899-5376-6_18 · Cited by 588 · 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
Komatsu, H., & Wurtz, R. H. (1988) · Journal of Neurophysiology · doi:10.1152/jn.1988.60.2.580 · Cited by 545 · see citing works
Self-citationDischarge characteristics of single units in superior colliculus of the alert rhesus monkey.
Schiller, P. H., & Koerner, F. (1971) · Journal of Neurophysiology · doi:10.1152/jn.1971.34.5.920 · Cited by 502 · see citing works
Unix-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
Mohler, C. W., & Wurtz, R. H. (1976) · Journal of Neurophysiology · doi:10.1152/jn.1976.39.4.722 · Cited by 456 · see citing works
Self-citationRichmond, B. J., Optican, L. M., Podell, M., & Spitzer, H. (1987) · Journal of Neurophysiology · doi:10.1152/jn.1987.57.1.132 · Cited by 428 · see citing works
Anatomical organization of pretectal nuclei and tectal laminae in the cat
Kanaseki, T., & Sprague, J. M. (1974) · The Journal of Comparative Neurology · doi:10.1002/cne.901580307 · Cited by 388 · see citing works
Sparks, D. L. (1978) · Brain Research · doi:10.1016/0006-8993(78)90075-6 · Cited by 386 · see citing works
The deep layers of the superior colliculus.
Sparks, D. L., & Hartwich‐Young, R. (1989) · PubMed · Cited by 359 · see citing works
Size and distribution of movement fields in the monkey superior colliculus
Sparks, D. L., Holland, R., & Guthrie, B. L. (1976) · Brain Research · doi:10.1016/0006-8993(76)90003-2 · Cited by 349 · see citing works
Signal Transformations Required For The Generation Of Saccadic Eye Movements
Sparks, D. L., & Mays, L. E. (1990) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.13.030190.001521 · Cited by 347 · see citing works
Distribution of acetyl cholinesterase in the hippocampal region of the guinea pig
Geneser-Jensen, F. A. (1972) · Cell and Tissue Research · doi:10.1007/bf00335257 · Cited by 311 · see citing works
A 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-citationStimulation of the superior colliculus in the alert cat
Guitton, D., Crommelinck, M., & Roucoux, A. (1980) · Experimental Brain Research · doi:10.1007/bf00237070 · Cited by 266 · see citing works
Moschovakis, A. K., Karabelas, A. B., & Highstein, S. M. (1988) · Journal of Neurophysiology · doi:10.1152/jn.1988.60.1.263 · Cited by 247 · see citing works
Superior Colliculus Cell Responses Related to Eye Movements in Awake Monkeys
Wurtz, R. H., & Goldberg, M. E. (1971) · Science · doi:10.1126/science.171.3966.82 · Cited by 245 · see citing works
Self-citationAnatomical organization of retinotectal afferents in the cat: An autodiographic study
Graybiel, A. M. (1975) · Brain Research · doi:10.1016/0006-8993(75)90566-1 · Cited by 238 · see citing works
Self-citationSuperior colliculus neurons provide the saccadic motor error signal
Waitzman, D. M., Ma, T. P., Optican, L. M., & Wurtz, R. H. (1988) · Experimental Brain Research · doi:10.1007/bf00250610 · Cited by 219 · see citing works
Self-citationMoschovakis, A. K., Karabelas, A. B., & Highstein, S. M. (1988) · Journal of Neurophysiology · doi:10.1152/jn.1988.60.1.232 · Cited by 211 · see citing works
Movement fields of saccade-related burst neurons in the monkey superior colliculus
Sparks, D. L., & Mays, L. E. (1980) · Brain Research · doi:10.1016/0006-8993(80)91158-0 · Cited by 201 · see citing works
The optic tracts and centers of the opossum. Didelphis virginiana
Tsai, C. (1925) · The Journal of Comparative Neurology · doi:10.1002/cne.900390202 · Cited by 175 · see citing works
Beninato, M., & Spencer, R. F. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902530409 · Cited by 158 · see citing works
Cholinergic innervation of the superior colliculus in the cat
Hall, W. C., Fitzpatrick, D., Klatt, L. L., & Raczkowski, D. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902870408 · Cited by 153 · see citing works
Hikosaka, O., & Wurtz, R. H. (1989) · PubMed · Cited by 136 · see citing works
Self-citationIlling, R., & Graybiel, A. M. (1985) · Neuroscience · doi:10.1016/0306-4522(85)90303-3 · Cited by 130 · see citing works
Self-citationSparks, D. L., & Porter, J. D. (1983) · Journal of Neurophysiology · doi:10.1152/jn.1983.49.1.64 · Cited by 125 · see citing works
The visual and frontal cortices.
Me, G., & Segraves, M. (1989) · PubMed · Cited by 99 · see citing works
Illing, R., & Graybiel, A. M. (1986) · Neuroscience · doi:10.1016/0306-4522(86)90160-0 · Cited by 90 · see citing works
Self-citationGraybiel, A. M. (1978) · Nature · doi:10.1038/272539b0 · Cited by 90 · see citing works
Self-citationNeuroanatomy of the oculomotor system. The reticular formation.
Büttner-Ennever, J. A., & Büttner, U. (1988) · PubMed · Cited by 86 · see citing works
A Phylogenetic Consideration of the Optic Tectum
Huber, G. C., & Crosby, E. C. (1933) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.19.1.15 · Cited by 79 · 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
Cluster-and-sheet pattern of enkephalin-like immunoreactivity in the superior colliculus of the cat
Graybiel, A. M., Brecha, N. C., & Karten, H. J. (1984) · Neuroscience · doi:10.1016/0306-4522(84)90147-7 · Cited by 63 · see citing works
Self-citationLaminar distribution and patchiness of cytochrome oxidase in mouse superior colliculus
Wiener, S. I. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902440202 · Cited by 57 · see citing works
Intermediate and deep layers of the macaque superior colliculus: A golgi study
Ma, T. P., Cheng, H. W., Czech, J. A., et al. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902950109 · Cited by 43 · see citing works
Self-citationLattices of high histochemical activity occur in the human, monkey, and cat superior colliculus
Wallack, M. N. (1988) · Neuroscience · doi:10.1016/0306-4522(88)90259-x · Cited by 33 · see citing works
The Anatomical Basis for Sensorimotor Transformations in the Superior Colliculus
Hall, W. C., & May, P. J. (1984) · Contributions to sensory physiology · doi:10.1016/b978-0-12-151808-0.50007-1 · Cited by 26 · see citing works
Origin of high acetylcholinesterase activity in the mouse superior colliculus
Wallace, M. N., & Fredens, K. (1988) · Experimental Brain Research · doi:10.1007/bf00250255 · Cited by 25 · see citing works
Illing, R. (1988) · Experimental Brain Research · doi:10.1007/bf00406618 · Cited by 17 · see citing works
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Lynch, J. C., Hoover, J. E., & Strick, P. L. (1994) · Experimental Brain Research · doi:10.1007/bf00227293 · Cited by 306 · see citing works
Freeman, S. M., & Young, L. J. (2016) · Journal of Neuroendocrinology · doi:10.1111/jne.12382 · Cited by 196 · see citing works
“Furthermore, cholinergic input from the PPT strongly innervates the macaque SC (53), and neurones in the PPT have also been shown to be active in monkeys during saccade tasks (54) and to directly stimulate SC neurones and facilitate the initiation of saccadic eye movements (55).”
BackgroundFreeman, S. M., Inoue, K., Smith, A. L., Goodman, M. M., & Young, L. J. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.03.023 · Cited by 185 · see citing works
“6), and cholinergic input from the PPT strongly innervates the macaque superior colliculus (SC) (Ma et al., 1991).”
BackgroundKobayashi, Y., Inoue, Y., Yamamoto, M., Isa, T., & Aizawa, H. (2002) · Journal of Neurophysiology · doi:10.1152/jn.2002.88.2.715 · Cited by 104 · see citing works
Freeman, S. M., Palumbo, M. C., Lawrence, R. H., Smith, A. L., Goodman, M. M., & Bales, K. L. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0315-3 · Cited by 82 · see citing works
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Salas, C., Herrero, L., Rodrı́guez, F., & Torres, B. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)83048-5 · Cited by 59 · see citing works
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Kobayashi, Y., Saito, Y., & Isa, T. (2001) · Brain and Development · doi:10.1016/s0387-7604(01)00330-8 · Cited by 26 · see citing works
- Authors
- Ma, T. P., Graybiel, A. M., & Wurtz, R. H.
- Affiliations
- National Institutes of Health (US)
- Massachusetts Institute of Technology (US)
- ORCID
- Graybiel, A.M.
- Venue
- Experimental Brain Research
- Published
- 1991-05
- Volume
- 85
- Issue
- 1
- Pages
- 21-35
- ISSN
- 0014-4819 (ISSN-L)
- 1432-1106
- OpenAlex
- W1969156877
- Cited by
- 71
- References
- 49
- Citations by year
- 2024: 1 · 2023: 1 · 2019: 1 · 2018: 3 · 2017: 2 · 2016: 2 · 2015: 4 · 2014: 2 · 2013: 2 · 2012: 3
- FWCI
- 2.35
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Experimental Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (1f32ey005950-01, 2r01ey002866-10a1)
- National Eye Institute (F32-EY05950, EY 5-RO1-EY02866-11)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Life Sciences › Neuroscience › Neurology › Vestibular and auditory disorders
- Keywords
- superior colliculus, rhesus monkeys, saccade programming, eye movements
- MeSH terms
- Acetylcholinesterase, Animals, Behavior, Animal, Macaca mulatta, Neurons, Saccades, Staining and Labeling, Stereotaxic Techniques, Superior Colliculi
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