Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-18T17:42:34.558Z Has data issue: false hasContentIssue false

Behavioral and electrophysiological sensitivity to temporally modulated visual stimuli in the ground squirrel

Published online by Cambridge University Press:  02 June 2009

Michael A. Crognale
Affiliation:
Department of Psychology, University of California, Santa Barbara
Gerald H. Jacobs
Affiliation:
Department of Psychology, University of California, Santa Barbara

Abstract

Behavioral and electrophysiological methods were used to measure sensitivity to flickering lights in a dichromatic species, the California ground squirrel (Spermophilus beecheyi). Discrimination tests were used to determine spectral sensitivity at stimulus frequencies from 5–50 Hz and increment threshold spectral sensitivity. The contributions of retinal mechanisms to these capacities were assessed by recording the responses of optic nerve fibers to temporally modulated monochromatic lights. In the ground squirrel, as in the human, the shape of the spectral-sensitivity function depends on the temporal frequency of the stimulus. Results from single-unit recording show that all of the classes of optic nerve fibers in the ground squirrel are highly phase-locked to the stimulus for modulation rates as high as 50 Hz. Neither the responses of photoreceptors nor any class of optic nerve fiber can singly account for the behavioral results. The electrophysiological results are also counter to models which propose that temporally dependent changes in the spectral sensitivity of spectrally opponent fibers account for the behavior. The temporal resolution of the optic nerve fibers exceeds that of the behaving animal suggesting that retinal mechanisms do not limit behavioral temporal resolution.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1991

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Baylor, D.A. (1986). Photoreceptor signals and vision. Investigative Ophthalmology and Visual Science 28, 3449.Google Scholar
Baylor, D.A., Nunn, B.J. & Schnapf, J.L. (1987). Spectral sensitivity of cones of the monkey (Macaca fascicularis). Journal of Physiology 390, 145160.CrossRefGoogle ScholarPubMed
Blakeslee, B. (1983). Electrophysiological studies of spectral mechanisms in the retinas of ground squirrels and tree squirrels. Doctoral Dissertation, University of California, Santa Barbara.Google Scholar
Bowling, D.B. (1989). Timing differences between the light responses of X cells recorded simultaneously in cat LGN. Visual Neuroscience 2, 383389.CrossRefGoogle Scholar
Boynton, R.M. & Baron, W. (1975). Sinusoidal flicker characteristics of primate cones to heterochromatic stimuli. Journal of the Optical Society of America 65, 10911100.CrossRefGoogle ScholarPubMed
Boynton, R.M. & Whitten, D.N. (1972). Selective chromatic adaptation in primate photoreceptors. Vision Research 12, 855874.CrossRefGoogle ScholarPubMed
Crognale, M. & Jacobs, G.H. (1988). Temporal response properties of the short-wavelength cone mechanism: comparison of receptor and postreceptor signals in the ground squirrel. Vision Research 28,10771082.CrossRefGoogle ScholarPubMed
Dawis, S.M. (1981). Polynomial expressions of pigment nomograms. Vision Research 21, 14271430.CrossRefGoogle ScholarPubMed
Derrington, A.M., Krauskopf, J. & Lennie, P. (1984). Chromatic mechanisms in lateral geniculate nucleus of macaque. Journal of Physiology 357, 241265.CrossRefGoogle ScholarPubMed
Derrington, A.M. & Lennie, P. (1984). Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. Journal of Physiology 357, 219240.CrossRefGoogle ScholarPubMed
De, Valois R.L., Albrecht, D.G. & Thorell, L.G. (1982). Spatial-frequency selectivity of cells in macaque visual cortex. Vision Research 22, 545559.Google Scholar
De, Valois R.L. & Jacobs, G.H. (1984). Neural mechanisms of color vision. In Handbook of Physiology. The Nervous System, Vol. III, Darian-Smith, I., pp. 425465. Baltimore, Maryland: Williams & Wilkens.Google Scholar
De, Valois R.L., Snodderly, D.M., Yund, E.W. & Hepler, N.K. (1977). Responses of macaque lateral geniculate cells to luminance and color figures. Sensory Processes 1, 244259.Google Scholar
Enroth-Cugell, C., Robson, J.G., Schweitzer-Tong, D.E. & Watson, A.B. (1983). Spatio-temporal interaction in cat retinal ganglion cells showing linear summation. Journal of Physiology 341, 279307.CrossRefGoogle Scholar
Gielen, C.C.A.M., Van, Gisbergen J.A.M. & Vendrick, A.J.H. (1982). Reconstruction of cone-system contributions to responses of colour-opponent neurones in monkey lateral geniculate. Biological Cybernetics 44, 211221.CrossRefGoogle ScholarPubMed
Gouras, P. & Eggers, H. (1982). Ganglion cells mediating the signals of blue-sensitive cones in primate retina detect white-yellow borders independently of brightness. Vision Research 22, 675679.CrossRefGoogle ScholarPubMed
Gouras, P. & Zrenner, E. (1979). Enhancement of luminance flicker by color-opponent mechanisms. Science 205, 587589.CrossRefGoogle Scholar
Gur, M. & Purple, R.L. (1979). Some temporal output properties of color-opponent units in the ground squirrel retina. Brain Research 166, 233244.CrossRefGoogle ScholarPubMed
Ikeda, M. & Boynton, R.M. (1962). Effect of test-flash duration on the spectral sensitivity of the eye. Journal of the Optical Society of America 52, 697699.CrossRefGoogle Scholar
Jacobs, G.H. (1983). Within-species variation in visual capacity among squirrel monkeys (Saimiri sciureus): sensitivity differences. Vision Research 23, 239248.CrossRefGoogle ScholarPubMed
Jacobs, G.H., Blakeslee, B., McCourt, M.E. & Tootell, R.B.H. (1980). Visual sensitivity of ground squirrels to temporal and luminance variations. Journal of Comparative Physiology 136, 291299.CrossRefGoogle Scholar
Jacobs, G.H., Blakeslee, B. & Tootell, R.B.H. (1981). Color-discrimination tests on fibers in ground squirrel optic nerve. Journal of Neurophysiology 45, 903914.CrossRefGoogle ScholarPubMed
Jacobs, G.H. & Tootell, R.B.H. (1980). Spectral-response properties of optic nerve fibers in the ground squirrel. Journal of Neurophysiology 45, 891902.CrossRefGoogle Scholar
Jacobs, G.H., Neitz, J. & Crognale, M. (1985). Spectral sensitivity of ground squirrel cones measured with ERG flicker photometry. Journal of Comparative Physiology A 156, 503509.CrossRefGoogle Scholar
Kelly, D.H. (1962). Visual responses to time-dependent stimuli, IV: Effects of chromatic adaptation. Journal of the Optical Society of America 52, 940.CrossRefGoogle ScholarPubMed
Kelly, D.H. (1975). Luminous and chromatic flickering patterns have opposite effects. Science 188, 371372.CrossRefGoogle ScholarPubMed
Kelly, D.H. & Van, Norren D. (1977). Two-band model of heterochromatic flicker. Journal of the Optical Society of America 67, 10811091.CrossRefGoogle ScholarPubMed
King-Smith, P.E. (1975). Visual detection analyzed in terms of luminance and chromatic signals. Nature (London) 255, 6970.CrossRefGoogle Scholar
King-Smith, P.E. & Carden, D. (1976). Luminance and opponent- color contributions to visual detection and adaptation and to temporal and spatial integration. Journal of the Optical Society of America 66, 709717.CrossRefGoogle ScholarPubMed
Kozak, W.M. & Reitboeck, H.J. (1974). Color-dependent distribution of spikes in single optic tract fibers of the cat. Vision Research 14, 405419.CrossRefGoogle ScholarPubMed
Kraft, T.W. (1988). Photocurrents of cone photoreceptors of the golden-mantled ground squirrel. Journal of Physiology 404, 199213.CrossRefGoogle ScholarPubMed
Lankheet, M.J.M., Molenarr, J. & Van, Der Grind W.A., (1989). The spike-generating mechanism of cat retinal ganglion cells. Vision Research 29, 505517.CrossRefGoogle ScholarPubMed
Lee, B.B., Martin, P.R. & Valberg, A. (1988). The physiological basis of heterochromatic flicker photometry demonstrated in the ganglion cells of the macaque retina. Journal of Physiology 404, 323347.CrossRefGoogle ScholarPubMed
Lee, J. & Stromeyer, C.F., 3, (1989). Contribution of human shortwave cones to luminance and motion detection. Journal of Physiology 413, 563593.CrossRefGoogle ScholarPubMed
Luce, R.D. (1959). Individual Choice Behavior. New York: Wiley.Google Scholar
Martin, P.R., Pokorny, J., Smith, V.C., Lee, B.B. & Valberg, A. (1989).Sensitivity of macaque ganglion cells to luminance and flicker. Investigative Ophthalmology and Visual Science (Suppl.) 30, 323.Google Scholar
Michael, C.R. (1968 a). Receptive fields of single optic nerve fibers in a mammal with an all cone retina, I: Contrast sensitive units. Journal of Neurophysiology 31, 249256.CrossRefGoogle Scholar
Michael, C.R. (1968 b). Receptive fields of single optic nerve fibers in a mammal with an all cone retina, III: Opponent color units. Journal of Neurophysiology 31, 268282.CrossRefGoogle Scholar
Mollon, J.D. & Polden, P.G. (1977). An anomaly in the response of the eye to light of short wavelengths. Philosophical Transactions of the Royal Society BM 278, 207240.Google ScholarPubMed
Sperling, H.G. & Harwerth, R.S. (1971). Red-green cone interactions in the increment-threshold spectral sensitivity of primates. Science, 172 28, 92.CrossRefGoogle ScholarPubMed
Van Norren, D. & Padmos, P. (1973). Human and macaque blue cones studied with electroretinography. Vision Research 13, 12411254.CrossRefGoogle Scholar
Wisowaty, J. & Boynton, R.M. (1980). Temporal modulation sensitivity of the blue mechanism: measurements made without chromatic adaptation. Vision Research 20, 895909.CrossRefGoogle ScholarPubMed
Yolton, R.L., Yolton, D.P., Renz, J. & Jacobs, G.H. (1974). Preretinal absorbance in sciurid eyes. Journal of Mammalogy 55, 1420.CrossRefGoogle ScholarPubMed
Zrenner, E. & Gouras, P. (1981), Characteristics of the blue-sensitive cone mechanism in primate retinal ganglion cells. Vision Research 21, 16051609.CrossRefGoogle ScholarPubMed