Skip to main content Accessibility help
×
×
Home

Comparison of contrast sensitivity in macaque monkeys and humans

  • William H. Ridder (a1), Kai Ming Zhang (a2), Apoorva Karsolia (a1), Michael Engles (a2) and James Burke (a2)...

Abstract

Contrast sensitivity functions reveal information about a subject’s overall visual ability and have been investigated in several species of nonhuman primates (NHPs) with experimentally induced amblyopia and glaucoma. However, there are no published studies comparing contrast sensitivity functions across these species of normal NHPs. The purpose of this investigation was to compare contrast sensitivity across these primates to determine whether they are similar. Ten normal humans and eight normal NHPs (Macaca fascicularis) took part in this project. Previously published data from Macaca mulatta and Macaca nemestrina were also compared. Threshold was operationally defined as two misses in a row for a descending method of limits. A similar paradigm was used for the humans except that the descending method of limits was combined with a spatial, two-alternative forced choice (2-AFC) technique. The contrast sensitivity functions were fit with a double exponential function. The averaged peak contrast sensitivity, peak spatial frequency, acuity, and area under the curve for the humans were 268.9, 3.40 cpd, 27.3 cpd, and 2345.4 and for the Macaca fascicularis were 99.2, 3.93 cpd, 26.1 cpd, and 980.9. A two-sample t-test indicated that the peak contrast sensitivities (P = 0.001) and areas under the curve (P = 0.010) were significantly different. The peak spatial frequencies (P = 0.150) and the extrapolated visual acuities (P = 0.763) were not different. The contrast sensitivities for the Macaca fascicularis, Macaca mulatta, and Macaca nemestrina were qualitatively and quantitatively similar. The contrast sensitivity functions for the NHPs had lower peak contrast sensitivities and areas under the curve than the humans. Even though different methods have been used to measure contrast sensitivity in different species of NHP, the functions are similar. The contrast sensitivity differences and similarities between humans and NHPs need to be considered when using NHPs to study human disease.

Copyright

Corresponding author

*Address correspondence to: William H. Ridder, III, Email: wridder@ketchum.edu

Footnotes

Hide All

Partial funding of this project was provided by Allergan.

Footnotes

References

Hide All
Abrahamsson, M., Fabian, G. & Sjostrand, J. (1992). Refraction changes in children developing convergent or divergent strabismus. British Journal of Ophthalmology 76, 723727.
Alexander, K.R., Barnes, C.S. & Fishman, G.A. (2003). Deficits in temporal integration for contrast processing in retinitis pigmentosa. Investigative Ophthalmology & Visual Science 44, 31633169.
Allman, J.M. (1977). Evolution of the visual system in the early primates. In Progress in Psychology and Physiological Psychology, ed. Sprague, J.M. & Epstein, A.N., pp. 153. New York: Academic Press.
Anand, V., Buckley, J.G., Scally, A. & Elliott, D.B. (2003). Postural stability changes in the elderly with cataract simulation and refractive blur. Investigative Ophthalmology & Visual Science 44, 46704675.
Bambo, M.P., Ferrandez, B., Guerri, N., Fuertes, I., Cameo, B., Polo, V., Larrosa, J.M. & Garcia-Martin, E. (2016). Evaluation of contrast sensitivity, chromatic vision, and reading ability in patients with primary open angle glaucoma. Journal of ophthalmology 2016, 7074016.
Barlow, H.B. (1958). Temporal and spatial summation in human vision at different background intensities. Journal of Physiology 141, 337350.
Boothe, R.G., Kiorpes, L. & Hendrickson, A. (1982). Anisometropic amblyopia in Macaca nemestrina monkeys produced by atropinization of one eye during development. Investigative Ophthalmology & Visual Science 22, 228233.
Burr, D.C. & Santoro, L. (2001). Temporal integration of optic flow, measured by contrast and coherence thresholds. Vision Research 41, 18911899.
Curcio, C.A., Medeiros, N.E. & Millican, C.L. (1996). Photoreceptor loss in age-related macular degeneration. Investigative Ophthalmology & Visual Science 37, 12361249.
De Valois, R.L., Morgan, H. & Snodderly, D.M. (1974). Psychophysical studies of monkey vision. 3. Spatial luminance contrast sensitivity tests of macaque and human observers. Vision Research 14, 7581.
Elliott, D.B. (2006). Contrast sensitivity and glare testing. In Borish’s Clinical Refraction (2nd ed.), ed. Benjamin, W.J., pp. 247288. St. Louis, MO: Butterworth.
Faria, B.M., Duman, F., Zheng, C.X., Waisbourd, M., Gupta, L., Ali, M., Zangalli, C., Lu, L., Wizov, S.S., Spaeth, E., Richman, J. & Spaeth, G.L. (2015). Evaluating contrast sensitivity in age-related macular degeneration using a novel computer-based test, the Spaeth/Richman contrast sensitivity test. Retina 35, 14651473.
Fernandes, A., Bradley, D.V., Tigges, M., Tigges, J. & Herndon, J.G. (2003). Ocular measurements throughout the adult life span of rhesus monkeys. Investigative Ophthalmology & Visual Science 44, 23732380.
Harwerth, R.S. (1982). Glenn Fry Award Lecture: Behavioral studies of amblyopia in monkeys. American Journal of Optometry and Physiological Optics 59, 535555.
Harwerth, R.S., Crawford, M.L., Smith, E.L. 3rd & Boltz, R.L. (1981). Behavioral studies of stimulus deprivation amblyopia in monkeys. Vision Research 21, 779789.
Harwerth, R.S. & Smith, E.L. 3rd (1985). Rhesus monkey as a model for normal vision of humans. American Journal of Optometry and Physiological Optics 62, 633641.
Harwerth, R.S., Smith, E.L. 3rd & Boltz, R.L. (1980). Meridional amblyopia in monkeys. Experimental Brain Research 39, 351356.
Harwerth, R.S., Smith, E.L. 3rd, Boltz, R.L., Crawford, M.L. & von Noorden, G.K. (1983). Behavioral studies on the effect of abnormal early visual experience in monkeys: Spatial modulation sensitivity. Vision Research 23, 15011510.
Harwerth, R.S., Smith, E.L. 3rd, Crawford, M.L. & von Noorden, G.K. (1984). Effects of enucleation of the nondeprived eye on stimulus deprivation amblyopia in monkeys. Investigative Ophthalmology & Visual Science 25, 1018.
Harwerth, R.S., Smith, E.L. 3rd, Crawford, M.L. & von Noorden, G.K. (1989). The effects of reverse monocular deprivation in monkeys. I. Psychophysical experiments. Experimental Brain Research 74, 327347.
Harwerth, R.S., Smith, E.L. 3rd, Duncan, G.C., Crawford, M.L. & von Noorden, G.K. (1986a). Effects of enucleation of the fixating eye on strabismic amblyopia in monkeys. Investigative Ophthalmology & Visual Science 27, 246254.
Harwerth, R.S., Smith, E.L. 3rd, Duncan, G.C., Crawford, M.L. & von Noorden, G.K. (1986b). Multiple sensitive periods in the development of the primate visual system. Science 232, 235238.
Harwerth, R.S., Smith, E.L. 3rd, Paul, A.D., Crawford, M.L. & von Noorden, G.K. (1991). Functional effects of bilateral form deprivation in monkeys. Investigative Ophthalmology & Visual Science 32, 23112327.
Hawkins, A.S., Szlyk, J.P., Ardickas, Z., Alexander, K.R. & Wilensky, J.T. (2003). Comparison of contrast sensitivity, visual acuity, and Humphrey visual field testing in patients with glaucoma. Journal of Glaucoma 12, 134138.
Haymes, S.A., Johnston, A.W. & Heyes, A.D. (2002). Relationship between vision impairment and ability to perform activities of daily living. Ophthalmic and Physiological Optics 22, 7991.
Hubel, D.H., Wiesel, T.N. & LeVay, S. (1976). Functional architecture of area 17 in normal and monocularly deprived macaque monkeys. Cold Spring Harbor Symposia on Quantitative Biology 40, 581589.
Kaas, J.H. (2007). Reconstructing the organization of neocortex of the first mammals and subsequent modifications. In Evolution of Nervous Systems: Mammals, ed. Kaas, J.H. & Krubitzer, L., pp. 2748. Oxford, UK: Elsevier.
Kiorpes, L., Boothe, R.G., Hendrickson, A.E., Movshon, J.A., Eggers, H.M. & Gizzi, M.S. (1987). Effects of early unilateral blur on the macaque’s visual system. I. Behavioral observations. Journal of Neuroscience 7, 13181326.
Kiorpes, L., Kiper, D.C. & Movshon, J.A. (1993). Contrast sensitivity and vernier acuity in amblyopic monkeys. Vision Research 33, 23012311.
Kleiner, R.C., Enger, C., Alexander, M.F. & Fine, S.L. (1988). Contrast sensitivity in age-related macular degeneration. Archives of Ophthalmology 106, 5557.
Krubitzer, L. (1995). The organization of neocortex in mammals: Are species differences really so different? Trends in Neurosciences 18, 408417.
Leat, S.J. & Woodhouse, J.M. (1993). Reading performance with low vision aids: Relationship with contrast sensitivity. Ophthalmic and Physiological Optics 13, 916.
Li, J., Spiegel, D.P., Hess, R.F., Chen, Z., Chan, L.Y., Deng, D., Yu, M. & Thompson, B. (2015). Dichoptic training improves contrast sensitivity in adults with amblyopia. Vision Research 114, 161172.
Lord, S.R. & Dayhew, J. (2001). Visual risk factors for falls in older people. Journal of the American Geriatrics Society 49, 508515.
McCann, J.J., Savoy, R.L., Hall, J.A. Jr. & Scarpetti, J.J. (1974). Visibility of continuous luminance gradients. Vision Research 14, 917927.
McKendrick, A.M., Sampson, G.P., Walland, M.J. & Badcock, D.R. (2007). Contrast sensitivity changes due to glaucoma and normal aging: Low-spatial-frequency losses in both magnocellular and parvocellular pathways. Investigative Ophthalmology & Visual Science 48, 21152122.
Meng, W., Butterworth, J., Malecaze, F. & Calvas, P. (2011). Axial length of myopia: A review of current research. Ophthalmologica 225, 127134.
Miller, M., Pasik, P. & Pasik, T. (1980). Extrageniculostriate vision in the monkey. VII. Contrast sensitivity functions. Journal of Neurophysiology 43, 15101526.
Mountcastle, V.B. (1978). An organizing principle for cerebral functions: The unit module and the distributed system. In The Mindful Brain, ed. Edelman, G.M., pp. 750. Cambridge, MA: MIT Press.
Nusinowitz, S., Ridder, W.H. 3rd & Ramirez, J. (2007). Temporal response properties of the primary and secondary rod-signaling pathways in normal and Gnat2 mutant mice. Experimental Eye Research 84, 11041114.
Owsley, C., Stalvey, B.T., Wells, J., Sloane, M.E. & McGwin, G. Jr (2001). Visual risk factors for crash involvement in older drivers with cataract. Archives of Ophthalmology 119, 881887.
Pelli, D.G. & Zhang, L. (1991). Accurate control of contrast on microcomputer displays. Vision Research 31, 13371350.
Ridder, W.H. 3rd & Nusinowitz, S. (2006). The visual evoked potential in the mouse–origins and response characteristics. Vision Research 46, 902913.
Robson, J.G. & Graham, N. (1981). Probability summation and regional variation in contrast sensitivity across the visual field. Vision Research 21, 409418.
Rockel, A.J., Hiorns, R.W. & Powell, T.P. (1980). The basic uniformity in structure of the neocortex. Brain 103, 221244.
Rogers, G.L., Bremer, D.L. & Leguire, L.E. (1987). The contrast sensitivity function and childhood amblyopia. American Journal of Ophthalmology 104, 6468.
Ross, J.E., Bron, A.J. & Clarke, D.D. (1984). Contrast sensitivity and visual disability in chronic simple glaucoma. British Journal of Ophthalmology 68, 821827.
Rubin, G.S., Roche, K.B., Prasada-Rao, P. & Fried, L.P. (1994). Visual impairment and disability in older adults. Optometry and Vision Science 71, 750760.
Smith, E.L. 3rd, Chino, Y.M., Ni, J., Cheng, H., Crawford, M.L. & Harwerth, R.S. (1997). Residual binocular interactions in the striate cortex of monkeys reared with abnormal binocular vision. Journal of Neurophysiology 78, 13531362.
Souza, G.S., Gomes, B.D. & Silveira, L.C. (2011). Comparative neurophysiology of spatial luminance contrast sensitivity. Psychology & Neurosciences 4, 2948.
Szentagothai, J. (1975). The ‘module-concept’ in cerebral cortex architecture. Brain Research 95, 475496.
Szlyk, J.P., Seiple, W., Fishman, G.A., Alexander, K.R., Grover, S. & Mahler, C.L. (2001). Perceived and actual performance of daily tasks: Relationship to visual function tests in individuals with retinitis pigmentosa. Ophthalmology 108, 6575.
Turano, K., Rubin, G.S., Herdman, S.J., Chee, E. & Fried, L.P. (1994). Visual stabilization of posture in the elderly: Fallers vs. nonfallers. Optometry and Vision Science 71, 761769.
Uhlrich, D.J., Essock, E.A. & Lehmkuhle, S. (1981). Cross-species correspondence of spatial contrast sensitivity functions. Behavioural Brain Research 2, 291299.
van Nes, F.L., Koenderink, J.J., Nas, H. & Bouman, M.A. (1967). Spatiotemporal modulation transfer in the human eye. Journal of the Optical Society of America 57, 10821088.
Weinreb, R.N., Aung, T. & Medeiros, F.A. (2014). The pathophysiology and treatment of glaucoma: A review. Jama 311, 19011911.
Wensveen, J.M., Harwerth, R.S., Hung, L.F., Ramamirtham, R., Kee, C.S. & Smith, E.L. 3rd (2006). Brief daily periods of unrestricted vision can prevent form-deprivation amblyopia. Investigative Ophthalmology & Visual Science 47, 24682477.
Wensveen, J.M., Smith, E.L. 3rd, Hung, L.F. & Harwerth, R.S. (2011). Brief daily periods of unrestricted vision preserve stereopsis in strabismus. Investigative Ophthalmology & Visual Science 52, 48724879.
Wiesel, T.N. & Raviola, E. (1979). Increase in axial length of the macaque monkey eye after corneal opacification. Investigative Ophthalmology & Visual Science 18, 12321236.
Williams, R.A. & Boothe, R.G. (1983). Effects of defocus on monkey (Macaca nemestrina) contrast sensitivity: Behavioral measurements and predictions. American Journal of Optometry and Physiological Optics 60, 106111.
Williams, R.A., Boothe, R.G., Kiorpes, L. & Teller, D.Y. (1981). Oblique effects in normally reared monkeys (Macaca nemestrina): Meridional variations in contrast sensitivity measured with operant techniques. Vision Research 21, 12531266.
Wood, J.M. & Troutbeck, R. (1994). Effect of visual impairment on driving. Human Factors 36, 476487.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Visual Neuroscience
  • ISSN: 0952-5238
  • EISSN: 1469-8714
  • URL: /core/journals/visual-neuroscience
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed