Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-23T13:47:21.677Z Has data issue: false hasContentIssue false

Temporal modulation sensitivity of tree shrew retinal ganglion cells

Published online by Cambridge University Press:  18 November 2003

HAIDONG D. LU
Affiliation:
Department of Psychological and Brain Sciences, University of Louisville, Louisville Present address: Department of Psychology, Vanderbilt University, 111 21st Avenue South, Nashville, TN 37203, USA.
HEYWOOD M. PETRY
Affiliation:
Department of Psychological and Brain Sciences, University of Louisville, Louisville Department of Opthalmology and Visual Sciences, University of Louisville, Louisville

Abstract

Tree shrews (Tupaia belangeri) are small diurnal mammals capable of quick and agile navigation. Electroretinographic and behavioral studies have indicated that tree shrews possess very good temporal vision, but the neuronal mechanisms underlying that temporal vision are not well understood. We used single-unit extracellular recording techniques to characterize the temporal response properties of individual retinal ganglion cell axons recorded from the optic tract. A prominent characteristic of most cells was their sustained or transient nature in responding to the flashing spot. Temporal modulation sensitivity functions were obtained using a Gaussian spot that was temporally modulated at different frequencies (2–60 Hz). Sustained cells respond linearly to contrast. They showed an average peak frequency of 6.9 Hz, a high-frequency cutoff at 31.3 Hz, and low-pass filtering. Transient cells showed nonlinear response to contrast. They had a peak frequency of 19.3 Hz, a high-frequency cutoff at about 47.6 Hz, band-pass filtering, and higher overall sensitivity than sustained cells. The responses of transient cells also showed a phase advance of about 88 deg whereas the phase advance for sustained cells was about 43 deg. Comparison with behavioral temporal modulation sensitivity results suggested that transient retinal ganglion cells may underlie detection for a wide range of temporal frequencies, with sustained ganglion cells possibly mediating detection below 4 Hz. These data suggest that two well-separated temporal channels exist at the retinal ganglion cell level in the tree shrew retina, with the transient channel playing a major role in temporal vision.

Type
Research Article
Copyright
2003 Cambridge University Press

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

REFERENCES

Ahnelt, P.K. & Kolb, H. (2000). The mammalian photoreceptor mosaic-adaptive design. Progress in Retinal and Eye Research 19, 711777.CrossRefGoogle Scholar
Awatramani, G.B. & Slaughter, M.M. (2000). Origin of transient and sustained responses in ganglion cells of the retina. Journal of Neuroscience 20, 70877095.Google Scholar
Benardete, E.A. & Kaplan, E. (1999). The dynamics of primate M retinal ganglion cells. Visual Neuroscience 16, 355368.CrossRefGoogle Scholar
Benardete, E.A., Kaplan, E., & Knight, B.W. (1992). Contrast gain control in the primate retina: P cells are not X-like, some M cells are. Visual Neuroscience 8, 483486.CrossRefGoogle Scholar
Bullier, J. & Norton, T.T. (1979). X and Y relay cells in the cat lateral geniculate nucleus: Quantitative analysis of receptive-field properties and classification. Journal of Neurophysiology 42, 244273.Google Scholar
Butler, P.M. (1972). The problem of insectivore classification. In Studies in Vertebrate Evolution, ed. Joysey, K.A. & Kemp, T.S., pp. 253265. Edinburgh, UK: Oliver and Boyd.
Callahan, T.L. & Petry, H.M. (2000). Psychophysical measurement of temporal modulation sensitivity in the tree shrew (Tupaia belangeri). Vision Research 40, 455458.CrossRefGoogle Scholar
Cleland, B.G., Dubin, M.W., & Levick, W.R. (1971). Sustained and transient neurons in the cat's retina and lateral geniculate nucleus. Journal of Physiology 217, 473496.CrossRefGoogle Scholar
Conley, M., Fitzpatrick, D., & Diamond, I.T. (1984). The laminar organization of the lateral geniculate body and the striate cortex in tree shrew (Tupaia glis). Journal of Neuroscience 4, 171197.Google Scholar
DeBruyn, E.J. (1983). The organization and central terminations of retinal ganglion cells in the tree shrew (Tupaia glis). Doctoral Dissertation, Vanderbilt University, Nashville, TN.
de Lange, H. (1954). Relationship between critical flicker frequency and a set of low-frequency characteristics of the eye. Journal of the Optical Society of America, A—Optics Image Science and Vision 44, 380389.CrossRefGoogle Scholar
de Lange, H. (1957). Attenuation characteristics and phase-shift characteristics of the human fovea-cortex system in relation to flicker-fusion phenomena. Doctoral Dissertation, Technische Hogeschool, Delft.
Derrington, A.M. & Lennie, P. (1984). Spatial and temporal contrast sensitivities of neurons in lateral geniculate nucleus of macaque. Journal of Physiology 357, 219240.CrossRefGoogle Scholar
DeVries, S. (2000). Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28, 847856.CrossRefGoogle Scholar
Dobkins, K.R., Anderson, C.M., & Lia, B. (1999). Infant temporal contrast sensitivity functions (tCSFs) mature earlier for luminance than for chromatic stimuli: Evidence for precocious magnocellular development? Vision Research 39, 32233239.Google Scholar
Drenhaus, U., Von Gunten, A., & Rager, G. (1997). Classes of axons and their distribution in the optic nerve of the tree shrew (Tupaia belangeri). Anatomical Record 249, 103116.3.0.CO;2-T>CrossRefGoogle Scholar
Enroth-Cugell, C. & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. Journal of Physiology 187, 517552.CrossRefGoogle Scholar
Freed, M.A. (2000). Parallel cone bipolar pathways to a ganglion cell use different rates and amplitudes of quantal excitation. Journal of Neuroscience 20, 39563963.Google Scholar
Freed, M.A. & Sterling, P. (1988). The ON-alpha ganglion cell of the cat retina and its presynaptic cell types. Journal of Neuroscience 8, 23032320.Google Scholar
Frishman, L.J., Freeman, A.W., Troy, J.B., Schweitzer-Tong, D.E., & Enroth-Cugell, C. (1987). Spatiotemporal frequency responses of cat retinal ganglion cells. Journal of General Physiology 89, 599628.CrossRefGoogle Scholar
Hartveit, E. & Heggelund, P. (1993). Brain-stem influence on visual response of lagged and nonlagged cells in the cat lateral geniculate nucleus. Visual Neuroscience 10, 325339.CrossRefGoogle Scholar
Hawken, M.J., Shapley, R.M., & Grosof, D.H. (1996). Temporal-frequency selectivity in monkey visual cortex. Visual Neuroscience 13, 477492.CrossRefGoogle Scholar
Hochstein, S. & Shapley, R.M. (1976a). Quantitative analysis of retinal ganglion cell classifications. Journal of Physiology 262, 237264.Google Scholar
Hochstein, S. & Shapley, R.M. (1976b). Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. Journal of Physiology 262, 265284.Google Scholar
Holdefer, R.N. & Norton, T.T. (1995). Laminar organization of receptive field properties in the dorsal lateral geniculate nucleus of the tree shrew (Tupaiaglis belangeri). Journal of Comparative Neurology 358, 401413.CrossRefGoogle Scholar
Humphrey, A.L. & Saul, A.B. (1992). Action of brain-stem reticular afferents on lagged and nonlagged cells in the cat lateral geniculate nucleus. Journal of Neurophysiology 68, 673691.Google Scholar
Humphrey, A.L. & Saul, A.B. (1993). The temporal transformation of retinal signals in the lateral geniculate nucleus of the cat: Implications for cortical function. In Thalamic Networks for Relay and Modulation, ed. Minciacchi, D., Molinari, M., Macchi, G. & Jones, E.G., pp. 8189. Oxford, UK: Pergamon Press.
Jacobs, G.H. & Neitz, J. (1986). Spectral mechanisms and color vision in the tree shrew (Tupaia belangeri). Vision Research 26, 291298.CrossRefGoogle Scholar
Kaplan, E. & Benardete, E. (2001). The dynamics of primate retinal ganglion cells. Progress in Brain Research 134, 1733.CrossRefGoogle Scholar
Kaplan, E. & Shapley, R. (1982). X and Y cells in the lateral geniculate nucleus of macaque monkeys. Journal of Physiology 330, 125143.CrossRefGoogle Scholar
Kaplan, E. & Shapley, R. (1986). The primate retina contains two types of ganglion cells, with high and low contrast sensitivity. Proceedings of the National Academy of Sciences of the U.S.A. 83, 27552757.CrossRefGoogle Scholar
Kelly, D.H. & Park, M. (1972). Flicker. In Handbook of Sensory Physiology, Vol. 7(4), ed. Jameson, D. & Hurvich, L.M., pp. 273302. Berlin: Springer.CrossRef
Kremers, J., Lee, B.B., Pokorny, J., & Smith, V.C. (1991). The response of macaque retinal ganglion cells to complex temporal waveforms. In From Pigments to Perception, ed. Valberg, A. & Lee, B.B., pp. 173176. New York: Plenum Press.CrossRef
Kremers, J., Lee, B.B., & Kaiser, P.K. (1992). Sensitivity of macaque retinal ganglion cells and human observers to combined luminance and chromatic temporal modulation. Journal of the Optical Society of America A—Optics Image Science and Vision 9, 14771485.CrossRefGoogle Scholar
Kuffler, S. (1953). Discharge patterns and functional organization of mammalian retina. Journal of Neurophysiology 16, 3768.Google Scholar
Langham, N.P.E. (1982). The ecology of the common tree shrew, Tupaia glis, in peninsular Malasia. Journal of Zoology 197, 323344.Google Scholar
Lankheet, M.J.M., Molenaar, J., & van de Grind, W.A. (1989). Frequency transfer properties of the spike generating mechanism of cat retinal ganglion cells. Vision Research 21, 16491661.CrossRefGoogle Scholar
Lee, B.B., Elepfandt, A., & Virsu, V. (1981). Phase of response to moving sinusoidal gratings in cells of cat retina and lateral geniculate nucleus. Journal of Neurophysiology 45, 807817.Google Scholar
Lee, B.B., Martin, P.R., & Valberg, A. (1989). Amplitude and phase of response of macaque ganglion cells to flickering stimuli. Journal of Physiology 414, 245263.CrossRefGoogle Scholar
Lee, B.B., Pokorny, J., Smith, V.C., Martin, P.R., & Valberg, A. (1990). Luminance and chromatic modulation sensitivity of macaque ganglion cells and human observers. Journal of the Optical Society of America A—Optics Image Science and Vision 7, 22232236.CrossRefGoogle Scholar
Lee, B.B., Martin, P.R., Valberg, A., & Kremers, J. (1993). Physiological mechanisms underlying psychophysical sensitivity to combined luminance and chromatic modulation. Journal of the Optical Society of America A—Optics Image Science and Vision 10, 14031412.CrossRefGoogle Scholar
Lee, B.B., Pokorny, J., Smith, V.C., & Kremers, J. (1994). Responses to pulses and sinusoids in macaque ganglion cells. Vision Research 34, 30813095.CrossRefGoogle Scholar
Lennie, P. (1980). Perceptual signs of parallel pathways. Philosophical Transactions of the Royal Society B (London) 290, 2327.CrossRefGoogle Scholar
Lu, H. & Petry, H.M. (2001). Temporal properties of single neurons in the tree shrew visual system: Comparisons from progressive levels of visual processing. Investigative Ophthalmology and Visual Science 42, S405.Google Scholar
Lu, S.M., Guido, W., Vaughan, J.W., & Sherman, S.M. (1995). Latency variability of responses to visual stimuli in cells of the cat's lateral geniculate nucleus. Experimental Brain Research 105, 717.Google Scholar
Luckett, W.P. (1980). Comparative Biology and Evolutionary Relationships of Tree Shrews. New York: Plenum Press.CrossRef
Mastronarde, D.N. (1987a). Two classes of single-input X-cells in cat lateral geniculate nucleus. I. Receptive-field properties and classification of cells. Journal of Neurophysiology 57, 357380.Google Scholar
Mastronarde, D.N. (1987b). Two classes of single-input X-cells in cat lateral geniculate nucleus. II. Retinal inputs and the generation of receptive-field properties. Journal of Neurophysiology 57, 381413.Google Scholar
Mastronarde, D.N., Humphrey, A.L., & Saul, A.B. (1991). Lagged Y cells in the cat lateral geniculate nucleus. Visual Neuroscience 7, 191200.CrossRefGoogle Scholar
Movshon, J.A., Thompson, I.D., & Tolhurst, D.J. (1978). Spatial and temporal contrast sensitivity of neurons in area 17 and 18 of the cat's visual cortex. Journal of Physiology 283, 101120.CrossRefGoogle Scholar
Müller, B. & Peichl, L. (1989). Topography of cones and rods in the tree shrew retina. Journal of Comparative Neurology 282, 581594.CrossRefGoogle Scholar
Naka, K.I. & Rushton, W.A. (1966). S-potentials from colour units in the retina of fish (Cyprinidae). Journal of Physiology 185, 536555.CrossRefGoogle Scholar
Norton, T.T. & Casagrande, V.A. (1982). Laminar organization of receptive-field properties in lateral geniculate nucleus of bush baby (Galago crassicaudatus). Journal of Neurophysiology 47, 715741.Google Scholar
Norton, T.T., Rager, G., & Kretz, R. (1985). On and Off regions in layer IV of striate cortex. Brain Research 327, 319323.CrossRefGoogle Scholar
Peichl, L., Ott, H., & Boycott, B.B. (1987). Alpha ganglion cells in mammalian retinae. Proceedings of the Royal Society B (London) 231, 169197.CrossRefGoogle Scholar
Perry, V.H., Oehler, R., & Cowey, A. (1984). Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey. Neuroscience 12, 11011123.CrossRefGoogle Scholar
Petry, H.M. & Hárosi, F.I. (1990). Visual pigments of the tree shrew (Tupaia Belangeri) and greater galago (Galago crassicaudatus): A microspectrophotometric investigation. Vision Research 30, 839851.CrossRefGoogle Scholar
Petry, H.M. & Kelly, J.P. (1991). Psychophysical measurement of spectral sensitivity and color vision in red-light-reared tree shrews (Tupaia belangeri). Vision Research 31, 17491757.CrossRefGoogle Scholar
Petry, H.M., Fox, R., & Casagrande, V.A. (1984). Spatial contrast sensitivity of the tree shrew. Vision Research 24, 10371042.CrossRefGoogle Scholar
Polson, M.C. (1968). Spectral sensitivity and color vision in Tupaia glis. Doctoral Dissertation, Indiana University, Bloomington, IN.
Robinson, D.W. & Chalupa, L.M. (1997). The intrinsic temporal properties of alpha and beta retinal ganglion cell are equivalent. Current Biology 7, 366374.CrossRefGoogle Scholar
Saul, A.B. & Humphrey, A.L. (1990). Spatial and temporal response properties of lagged and nonlagged cells in cat lateral geniculate nucleus. Journal of Neurophysiology 64, 206224.Google Scholar
Saul, A.B. & Humphrey, A.L. (1992). Temporal-frequency tuning of direction selectivity in cat visual cortex. Visual Neuroscience 8, 365372.CrossRefGoogle Scholar
Schafer, D. (1969). Experiments on the physiology of the eye of the tree shrew Tupaia glis. Journal of Comparative Physiology 63, 204226.Google Scholar
Schiller, P.H. & Malpeli, J.G. (1977). Properties and tectal projections of monkey retinal ganglion cells. Journal of Neurophysiology 40, 428445.Google Scholar
Schiller, P.H. & Malpeli, J.G. (1978). Functional specificity of lateral geniculate nucleus laminae of the rhesus monkey. Journal of Neurophysiology 41, 788797.Google Scholar
Schiller, P.H., Finlay, B.L., & Volman, S.F. (1976). Quantitative studies of single-cell properties in monkey striate cortex. I. Spatiotemporal organization of receptive fields. Journal of Neurophysiology 39, 12881319.Google Scholar
Sclar, G. (1987). Expression of “retinal” contrast gain control by neurons of the cat's lateral geniculate nucleus. Experimental Brain Research 66, 589596.CrossRefGoogle Scholar
Shapley, R. & Perry, V.H. (1986). Cat and monkey retinal ganglion cells and their visual functional roles. Trends in Neuroscience 9, 229235.CrossRefGoogle Scholar
Shapley, R.M. & Victor, J.D. (1978). The effect of contrast on the transfer properties of cat retinal ganglion cells. Journal of Physiology 285, 275298.CrossRefGoogle Scholar
Shapley, R.M. & Victor, J.D. (1979). Nonlinear spatial summation and the contrast gain control of cat retinal ganglion cells. Journal of Physiology 290, 141161.CrossRefGoogle Scholar
Sherman, S.M., Norton, T.T., & Casagrande, V.A. (1975). X- and Y-cells in the dorsal lateral geniculate nucleus of the tree shrew (Tupaia glis). Brain Research 93, 152157.CrossRefGoogle Scholar
Silveira, L.C. & Perry, V.H. (1991). The topography of magnocellular projecting ganglion cells (M-ganglion cells) in the primate retina. Neuroscience 40, 217237.CrossRefGoogle Scholar
Sturr, J.F. & Shansky, M.S. (1971). Cortical and subcortical responses to flicker in cats. Experimental Neurology 33, 279290.Google Scholar
ter Laak, H.J. & Thijssen, J.M. (1978). Receptive field properties of optic tract fibers from on-center sustained and transient cells in a tree shrew (Tupaia chinensis). Vision Research 18, 10971109.Google Scholar
Thijssen, J.M., van Dongen, P.A.M., & ter Laak, H.J. (1976). Maintained activity of cells in the tree shrew's optic tract. Experimental Brain Research 25, 279290.Google Scholar
Tigges, J., Brooks, B.A., & Klee, M.R. (1967). ERG recordings of a primate pure cone retina (Tupaia glis). Vision Research 7, 553563.Google Scholar
Troy, J.B. & Shou, T. (2002). The receptive fields of cat retinal ganglion cells in physiological and pathological states: Where we are after half a century of research. Progress in Retinal Research 21, 263302.Google Scholar
Uhlrich, D.J., Tamamaki, N., & Sherman, M. (1990). Brainstem control of response modes in neurons of the cat's lateral geniculate nucleus. Proceedings of the National Academy of Sciences of the U.S.A. 87, 25602563.Google Scholar
van Dongen, P.A.M., ter Laak, H.J., Thijssen, J.M., & Vendrik, A.J.H. (1976). Functional classification of cells in the optic tract of a tree shrew (Tupaia chinensis). Experimental Brain Research 24, 441446.Google Scholar
Victor, J.D. (1987). The dynamics of the cat retinal X-cell center. Journal of Physiology 386, 219246.Google Scholar
Victor, J.D. & Shapley, R.M. (1979). Receptive field mechanisms of cat X and Y retinal ganglion cells. Journal of General Physiology 74, 275298.Google Scholar
Watanabe, M. & Rodieck, R.W. (1989). Parasol and midget ganglion cells of the primate retina. Journal of Comparative Neurology 289, 434454.Google Scholar
Werblin, F.S. & Dowling, J.E. (1969). Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. Journal of Neurophysiology 32, 339355.Google Scholar
Wilson, H.R. (1978). Quantitative prediction of line spread function measurements: Implications for channel bandwidths. Vision Research 18, 493496.Google Scholar
Wolfe, J.M. & Palmer, L.A. (1998). Temporal diversity in the lateral geniculate nucleus of cat. Visual Neuroscience 15, 653675.Google Scholar
Yeh, T., Lee, B.B., Kremers, J., Cowing, J.A., Hunt, D.M., Martin, P.R., & Troy, J.B. (1995). Visual responses in the lateral geniculate nucleus of dichromatic and trichromatic marmosets (Callithrix jacchus). Journal of Neuroscience 15, 78927904.Google Scholar