Skip to main content Accessibility help

Temporal-frequency selectivity in monkey visual cortex

  • M. J. Hawken (a1), R. M. Shapley (a1) and D. H. Grosof (a1)


We investigated the dynamics of neurons in the striate cortex (V1) and the lateral geniculate nucleus (LGN) to study the transformation in temporal-frequency tuning between the LGN and V1. Furthermore, we compared the temporal-frequency tuning of simple with that of complex cells and direction-selective cells with nondirection-selective cells, in order to determine whether there are significant differences in temporal-frequency tuning among distinct functional classes of cells within V1. In addition, we compared the cells in the primary input layers of V1 (4a, 4cα, and 4cβ) with cells in the layers that are predominantly second and higher order (2, 3, 4b, 5, and 6). We measured temporal-frequency responses to drifting sinusoidal gratings. For LGN neurons and simple cells, we used the amplitude and phase of the fundamental response. For complex cells, the elevation of impulse rate (F0) to a drifting grating was the response measure. There is significant low-pass filtering between the LGN and the input layers of V1 accompanied by a small, 3-ms increase in visual delay. There is further low-pass filtering between V1 input layers and the second- and higher-order neurons in V1. This results in an average decrease in high cutoff temporal-frequency between the LGN and V1 output layers of about 20 Hz and an increase in average visual latency of about 12–14 ms. One of the most salient results is the increased diversity of the dynamic properties seen in V1 when compared to the cells of the lateral geniculate, possibly reflecting specialization of function among cells in V1. Simple and complex cells had distributions of temporal-frequency tuning properties that were similar to each other. Direction-selective and nondirection-selective cells had similar preferred and high cutoff temporal frequencies, but direction-selective cells were almost exclusively band-pass while nondirection-selective cells distributed equally between band-pass and low-pass categories. Integration time, a measure of visual delay, was about 10 ms longer for V1 than LGN. In V1 there was a relatively broad distribution of integration times from 40–80 ms for simple cells and 60–100 ms for complex cells while in the LGN the distribution was narrower.



Hide All
Anderson, S.J. & Burr, D.C. (1985). Spatial and temporal selectivity of the human motion detecting system. Vision Research 25, 11471154.
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.
Breitmeyer, B. (1984). Visual masking. Oxford: Oxford University Press.
Brenner, D., Shapley, R.M. & Kaplan, E. (1981). Temporal integration in the visual system of the cat and the monkey. Society of Neuroscience Abstracts 7, 559.
Bullier, J. & Henry, G.H. (1980). Ordinal position and afferent input of neurons in monkey striate cortex. Journal of Comparative Neurology 193, 913935.
Derrington, A.M. & Lennie, P. (1984). Spatial and temporal contrast sensitivities of neurones in the lateral geniculate nucleus of the macaque. Journal of Physiology 357, 219240.
DeValois, R.L., Albrecht, D.G. & Thorell, L.G. (1982). Spatial frequency selectivity of cells in macaque visual cortex. Vision Research 22, 545559.
DeYoe, E.A. & Van Essen, D.C. (1988). Concurrent processing streams in monkey visual cortex. Trends in Neuroscience 11, 219226.
Felleman, D.J. & Van Essen, D.C. (1991). Distributed hierarchical processing in primate cerebral cortex. Cerebral Cortex 1, 147.
Foster, K.H., Gaska, J.P., Nagler, M. & Pollen, D.A. (1985). Spatial and temporal frequency selectivity of neurons in visual cortical areas V1 and V2 of the macaque monkey. Journal of Physiology 365, 331363.
Hamilton, D.B., Albrecht, D.G. & Geisler, W.S. (1989). Visual cortical receptive fields in monkey and cat: Spatial and temporal phase transfer function. Vision Research 29, 12851308.
Harwerth, R.S., Smith, E.L., Bolt, R.L., Crawford, M.L.J. & von Noorden, G.K. (1983). Behavioral studies on the effect of abnormal early visual experience in monkeys: Temporal modulation sensitivity. Vision Research 23, 15111517.
Hawken, M.J. & Parker, A.J. (1987). Spatial properties of neurons in the monkey striate cortex. Proceedings of the Royal Society B. (London) 231, 251288.
Hawken, M.J., Parker, A.J. & Lund, J.S. (1988). Laminar organization and contrast sensitivity of direction selective cells in the striate cortex of the old world monkey. Journal of Neuroscience 8, 35413548.
Hawken, M.J., Shapley, R.M., Gordon, J., Grosof, D.H. & Mechler, F. (1994). Comparison of temporal tuning in primate geniculate and V1. Investigative Ophthalmology and Visual Science (Suppl.) 35, 1662.
Heeger, D.J. (1987). Model for the extraction of image flow. Journal of the Optical Society of America A 4, 14551471.
Hess, R.F. & Snowden, R.J. (1992). Temporal properties of human visual filters: number, shapes, and spatial covariation. Vision Research 32, 4759.
Hicks, T.P., Lee, B.B. & Vidyasagar, T.R. (1983). The responses of cells in the macaque lateral geniculate nucleus to sinusoidal gratings. Journal of Physiology 337, 183200.
Hubel, D.H. & Wiesel, T.N. (1968). Receptive fields and functional architecture of monkey striate cortex. Journal of Physiology 195, 215243.
Kaplan, E. & Shapley, R.M. (1982). X & Y cells in the lateral geniculate nucleus of macaque monkeys. Journal of Physiology 330, 125143.
Kelly, D.H. (1971 a). Theory of flicker and transient responses I. Uniform fields. Journal of the Optical Society of America 61, 537546.
Kelly, D.H. (1971 b). Theory of flicker and transient responses II. Counterphase gratings. Journal of the Optical Society of America 61, 632640.
Kelly, D.H. (1979). Motion and Vision 11. Stabilized spatiolemporal threshold surface. Journal of the Optical Society of America 69, 13401349.
Kremers, J., Lee, B.B., Pokorny, J. & Smith, V.C. (1993). Responses of macaque ganglion cells and human observers to compound periodic waveforms. Vision Research 33, 19972011.
Lee, B.B., Martin, P.R. & Valberg, A. (1989). Sensitivity of macaque retinal ganglion cells to chromatic and luminance flicker. Journal of Physiology 414, 245263.
Lennie, P., Krauskopf, J. & Sclar, G. (1990). Chromatic mechanisms in striate cortex of macaque. Journal of Neuroscience 10, 649669.
Levitt, J.B., Kiper, D.C. & Movshon, J.A. (1994). Receptive fields and functional architecture of macaque V2. Journal of Neurophysiology 71, 25172542.
Livingstone, M.S. & Hubel, D.H. (1987). Psychophysical evidence for separate channels for the perception of form, color, movement and depth. Journal of Neuroscience 7, 34163468.
Lund, J.S. (1988). Anatomical organization of macaque monkey striate cortex. Annual Review of Neuroscience 11, 253288.
Maffei, L. & Fiorentini, A. (1973). The visual cortex as a spatial frequency analyzer. Vision Research 13, 12551268.
Mandler, M.B. & Makous, W. (1984). A three channel model of temporal frequency perception. Vision Research 24, 18811887.
Maunsell, J.H.R. & Gibson, J.R. (1992). Visual response latencies in striate cortex of the macaque monkey. Journal of Neurophysiology 68, 13321344.
Merigan, W.H. & Maunsell, J.H.R. (1993). How parallel are the primate visual pathways? Annual Review of Neuroscience 16, 369402.
Merigan, W.H., Byrne, C. & Maunsell, J.H.R. (1991). Does primate motion vision depend on the magnocellular pathway? Journal of Neuroscience 11, 34223429.
Merrill, E.G. & Ainsworth, A. (1972). Glass-coated platinum-plated tungsten microelectrodes. Medical and Biological Engineering 10, 662672.
Milkman, N., Schick, G., Rossetto, M., Ratliff, F., Shapley, R.M. & Victor, J.D. (1980). A two dimensional computer controlled visual stimulator. Behavioral Research Methods and Instrumentation 12, 283292.
Movshon, J.A., Thompson, I.D. & Tolhurst, D.J. (1978 a). Spatial summation in the receptive fields of simple cells in the cat's striale cortex. Journal of Physiology 283, 5377.
Movshon, J.A., Thompson, I.D. & Tolhurst, D.J. (1978 b). Spatial summation in the receptive fields of simple cells in the cat's striate cortex. Journal of Physiology 283, 7999.
Reid, R.C., Victor, J.D. & Shapley, R.M. (1992). Broadband temporal stimuli decrease the integration time of neurons in cat striate cortex. Visual Neuroscience 9, 3945.
Robson, J.G. (1966). Spatial and temporal contrast-sensitivity functions of the visual system. Journal of the Optical Society of America 56, 11411142.
Shapley, R.M. (1990). Parallel retinocortical channels. In Applications of Parallel Processing in Vision, ed. Brannan, J., pp. 336. Amsterdam: Elsevier.
Skottun, B.C., DeValois, R.L., Grosof, D.H., Movshon, J.A., Albrecht, D.G. & Bonds, A.B. (1991). Classifying simple and complex cells on the basis of response modulation. Vision Research 31, 10791086.
Smith, A.T. & Edgar, G.K. (1994). Antagonistic comparison of temporal frequency filter outputs as a basis for speed perception. Vision Research 34, 253265.
Snedecor, G.W. & Cochran, W.G. (1980). Statistical Methods, 7th edition. Ames, Iowa: Iowa State University Press.
Spekreijse, H., Estevez, O. & Reits, D. (1977). Visual evoked potentials and the physiological analysis of visual processes in man. In Visual Evoked Potentials in Man, ed. Desmedt, J.E., pp. 1689. Oxford: Oxford University Press.
Williamson, S.J., Kaufman, L. & Brenner, D. (1978). Latency of the neuromagnetic response of the human visual cortex. Vision Research 18, 107110.
Wong-Riley, M. (1979). Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Research 171, 1128.
Zeki, S.M. (1980). Functional organization of the cerebral cortex in the rhesus monkey. Nature 274, 423428.



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