Skip to main content Accessibility help
×
Home

Temporal-frequency selectivity in monkey visual cortex

Published online by Cambridge University Press:  02 June 2009

M. J. Hawken
Affiliation:
Center for Neural Science, New York University, New York
R. M. Shapley
Affiliation:
Center for Neural Science, New York University, New York
D. H. Grosof
Affiliation:
Center for Neural Science, New York University, New York

Abstract

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.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below.

References

Anderson, S.J. & Burr, D.C. (1985). Spatial and temporal selectivity of the human motion detecting system. Vision Research 25, 11471154.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 ScholarPubMed
Breitmeyer, B. (1984). Visual masking. Oxford: Oxford University Press.Google Scholar
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.Google Scholar
Bullier, J. & Henry, G.H. (1980). Ordinal position and afferent input of neurons in monkey striate cortex. Journal of Comparative Neurology 193, 913935.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
DeValois, R.L., Albrecht, D.G. & Thorell, L.G. (1982). Spatial frequency selectivity of cells in macaque visual cortex. Vision Research 22, 545559.CrossRefGoogle Scholar
DeYoe, E.A. & Van Essen, D.C. (1988). Concurrent processing streams in monkey visual cortex. Trends in Neuroscience 11, 219226.CrossRefGoogle ScholarPubMed
Felleman, D.J. & Van Essen, D.C. (1991). Distributed hierarchical processing in primate cerebral cortex. Cerebral Cortex 1, 147.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
Heeger, D.J. (1987). Model for the extraction of image flow. Journal of the Optical Society of America A 4, 14551471.CrossRefGoogle ScholarPubMed
Hess, R.F. & Snowden, R.J. (1992). Temporal properties of human visual filters: number, shapes, and spatial covariation. Vision Research 32, 4759.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1968). Receptive fields and functional architecture of monkey striate cortex. Journal of Physiology 195, 215243.CrossRefGoogle ScholarPubMed
Kaplan, E. & Shapley, R.M. (1982). X & Y cells in the lateral geniculate nucleus of macaque monkeys. Journal of Physiology 330, 125143.CrossRefGoogle Scholar
Kelly, D.H. (1971 a). Theory of flicker and transient responses I. Uniform fields. Journal of the Optical Society of America 61, 537546.CrossRefGoogle ScholarPubMed
Kelly, D.H. (1971 b). Theory of flicker and transient responses II. Counterphase gratings. Journal of the Optical Society of America 61, 632640.CrossRefGoogle ScholarPubMed
Kelly, D.H. (1979). Motion and Vision 11. Stabilized spatiolemporal threshold surface. Journal of the Optical Society of America 69, 13401349.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Lennie, P., Krauskopf, J. & Sclar, G. (1990). Chromatic mechanisms in striate cortex of macaque. Journal of Neuroscience 10, 649669.CrossRefGoogle ScholarPubMed
Levitt, J.B., Kiper, D.C. & Movshon, J.A. (1994). Receptive fields and functional architecture of macaque V2. Journal of Neurophysiology 71, 25172542.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Lund, J.S. (1988). Anatomical organization of macaque monkey striate cortex. Annual Review of Neuroscience 11, 253288.CrossRefGoogle Scholar
Maffei, L. & Fiorentini, A. (1973). The visual cortex as a spatial frequency analyzer. Vision Research 13, 12551268.CrossRefGoogle Scholar
Mandler, M.B. & Makous, W. (1984). A three channel model of temporal frequency perception. Vision Research 24, 18811887.CrossRefGoogle ScholarPubMed
Maunsell, J.H.R. & Gibson, J.R. (1992). Visual response latencies in striate cortex of the macaque monkey. Journal of Neurophysiology 68, 13321344.CrossRefGoogle ScholarPubMed
Merigan, W.H. & Maunsell, J.H.R. (1993). How parallel are the primate visual pathways? Annual Review of Neuroscience 16, 369402.CrossRefGoogle ScholarPubMed
Merigan, W.H., Byrne, C. & Maunsell, J.H.R. (1991). Does primate motion vision depend on the magnocellular pathway? Journal of Neuroscience 11, 34223429.CrossRefGoogle Scholar
Merrill, E.G. & Ainsworth, A. (1972). Glass-coated platinum-plated tungsten microelectrodes. Medical and Biological Engineering 10, 662672.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Robson, J.G. (1966). Spatial and temporal contrast-sensitivity functions of the visual system. Journal of the Optical Society of America 56, 11411142.CrossRefGoogle Scholar
Shapley, R.M. (1990). Parallel retinocortical channels. In Applications of Parallel Processing in Vision, ed. Brannan, J., pp. 336. Amsterdam: Elsevier.Google Scholar
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.CrossRefGoogle ScholarPubMed
Smith, A.T. & Edgar, G.K. (1994). Antagonistic comparison of temporal frequency filter outputs as a basis for speed perception. Vision Research 34, 253265.CrossRefGoogle ScholarPubMed
Snedecor, G.W. & Cochran, W.G. (1980). Statistical Methods, 7th edition. Ames, Iowa: Iowa State University Press.Google Scholar
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.Google Scholar
Williamson, S.J., Kaufman, L. & Brenner, D. (1978). Latency of the neuromagnetic response of the human visual cortex. Vision Research 18, 107110.CrossRefGoogle ScholarPubMed
Wong-Riley, M. (1979). Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Research 171, 1128.CrossRefGoogle ScholarPubMed
Zeki, S.M. (1980). Functional organization of the cerebral cortex in the rhesus monkey. Nature 274, 423428.CrossRefGoogle Scholar

Full text views

Full text views reflects PDF downloads, PDFs sent to Google Drive, Dropbox and Kindle and HTML full text views.

Total number of HTML views: 0
Total number of PDF views: 144 *
View data table for this chart

* Views captured on Cambridge Core between September 2016 - 19th January 2021. This data will be updated every 24 hours.

Hostname: page-component-77fc7d77f9-95hzn Total loading time: 0.298 Render date: 2021-01-19T03:00:53.952Z Query parameters: { "hasAccess": "0", "openAccess": "0", "isLogged": "0", "lang": "en" } Feature Flags last update: Tue Jan 19 2021 02:56:46 GMT+0000 (Coordinated Universal Time) Feature Flags: { "metrics": true, "metricsAbstractViews": false, "peerReview": true, "crossMark": true, "comments": true, "relatedCommentaries": true, "subject": true, "clr": true, "languageSwitch": true, "figures": false, "newCiteModal": false, "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true }

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Temporal-frequency selectivity in monkey visual cortex
Available formats
×

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

Temporal-frequency selectivity in monkey visual cortex
Available formats
×

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

Temporal-frequency selectivity in monkey visual cortex
Available formats
×
×

Reply to: Submit a response


Your details


Conflicting interests

Do you have any conflicting interests? *