Hostname: page-component-8448b6f56d-c4f8m Total loading time: 0 Render date: 2024-04-23T08:46:59.478Z Has data issue: false hasContentIssue false
  • English
  • Français

Quadrature subunits in directionally selective simple cells: Counterphase and drifting grating responses

Published online by Cambridge University Press:  02 June 2009

Robert C. Emerson  and
Morgan C. Huang
Robert C. Emerson
Affiliation:
Department of Ophthalmology and Center for Visual Science, University of Rochester, Rochester, New York
Morgan C. Huang
Affiliation:
Department of Ophthalmology, University of Rochester, Rochester
Get access Rights & Permissions [Opens in a new window]

Abstract

Here we examine further the basis for directional selectivity (DS) in simple cells of the cat's striate cortex. We use a distinctly different input stimulus and different analysis of the output signal for the same type of space-time inseparable receptive field (RF) that was measured with flashing bars in the companion paper (Emerson, 1997). As in the companion paper, we have mimicked a popular “linear” model with a single “branch” that consists of a linear spatiotemporal filter followed by a soft threshold, which should mimic any simple cells that have a single subunit. Counterphase sinusoidal measurements of such a configuration always generate elliptically shaped polar plots of amplitude versus temporal phase, often pinched along the minor axis because of a high threshold. However, for many spatiotemporal frequencies, such polar phase plots, as measured in simple cells by others, show a consistent rotational phase skew. Here we apply counterphase analysis to the same 2-branch model as developed in the companion paper. We show that the model accounts for the skew as the summation of signals from linear filters separated spatially and temporally by approximately 90 deg (i.e. in spatiotemporal phase quadrature), each separated from the output stage by a soft-threshold nonlinearity. We also prove conclusively that such skew cannot be generated by a single-subunit configuration. This demonstration supports the proposed two-subunit structure for DS simple cells, such as in the example from the companion paper, which has strong linear contributions from its inseparable RF. The presence of at least two nonlinear subunits appears to be an obligatory concomitant of DS in all visual cortical cells. The primary function of these subunits may be to enhance the strength of responses to images moving in the preferred direction, as in complex cells. However, subunits may also aid in identifying the moving object through overcoming, at least partially, the phase-concealing properties of the neuron's threshold by generating a steady signal that effectively decreases the threshold for the preferred direction.

Keywords

Directional selectivityReceptive-field subunitsNonlinear mechanismsSimple-cell modelsCounterphase responses
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 2 , March 1997 , pp. 373 - 385
Copyright
Copyright © Cambridge University Press 1997

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

Adelson, E.H. & Bergen, J.R. (1985). Spatiotemporal energy models for the perception of motion. Journal of the Optical Society of America A 2, 284–299.CrossRefGoogle ScholarPubMed
Albrecht, D.G. & Geisler, W.S. (1991). Motion selectivity and the contrast-response function of simple cells in the visual cortex. Visual Neuroscience 7, 531–546.CrossRefGoogle ScholarPubMed
Bauman, L.A. & Bonds, A.B. (1991). Inhibitory refinement of spatial frequency selectivity in single cells of the cat striate cortex. Vision Research 31, 933–944.CrossRefGoogle ScholarPubMed
Bonds, A.B. (1991). Temporal dynamics of contrast gain in single cells of the cat striate cortex. Visual Neuroscience 6, 239–255.CrossRefGoogle ScholarPubMed
Carandini, M., Heeger, D.J., O'Keefe, L.P., Movshon, J.A. & Tang, C. (1994). Simple cells, spatiotemporal frequency and contrast. Investigative Ophthalmology and Visual Science (Suppl.) 35, 1469.Google Scholar
DeAngelis, G.C., Ohzawa, I. & Freeman, R.D. (1993). Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. II. Linearity of temporal and spatial summation. Journal of Neurophysiology 69, 1118–1135.CrossRefGoogle ScholarPubMed
Emerson, R.C., Citron, M.C., Vaughn, W.J. & Klein, S.A. (1987). Nonlinear directionally selective subunits in complex cells of cat striate cortex. Journal of Neurophysiology 58, 33–65.CrossRefGoogle ScholarPubMed
Emerson, R.C., Korenberg, M.J. & Citron, M.C. (1989). Identification of intensive nonlinearities in cascade models of visual cortex and its relation to cell classification. In Advanced Methods of Physiological System Modeling, ISBN 0–306–43259–5, ed. Marmarelis, V.Z., pp. 97–111. New York: Plenum Press.CrossRefGoogle Scholar
Emerson, R.C. & Citron, M.C. (1992). Linear and nonlinear mechanisms of motion selectivity in simple cells of the cat's striate cortex. In Non-linear Vision: Determination of Neural Receptive Fields, Function, and Networks, ed. Pinter, R.B. & Nabet, B., pp. 75–89. Boca Raton, Florida: CRC Press.Google Scholar
Emerson, R.C., Korenberg, M.J. & Citron, M.C. (1992 a). Identification of complex-cell intensive nonlinearities in a cascade model of cat visual cortex. Biological Cybernetics 66, 291–300.CrossRefGoogle Scholar
Emerson, R.C., Bergen, J.R. & Adelson, E.H. (1992 b). Directionally selective complex cells and the computation of motion energy in cat visual cortex. Vision Research 32, 203–218.CrossRefGoogle ScholarPubMed
Emerson, R.C. & Maher, S.J. (1994). Hidden subunits may explain strength of directional selectivity in simple cells of striate cortex. Investigative Ophthalmology and Visual Science (Suppl.) 35, 1469.Google Scholar
Emerson, R.C. (1995). Directional selectivity in striate cortex needs nonlinear spatiotemporal interactions, even in a spatially odd-symmetric simple cell. Investigative Ophthalmology and Visual Science (Suppl.) 36, S873.Google Scholar
Emerson, R.C. (1997). Quadrature subunits in directionally selective simple cells: Spatiotemporal interactions. Visual Neuroscience 14, 357–371.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. Journal of Physiology (London) 187, 517–552.CrossRefGoogle ScholarPubMed
Heeger, D.J. (1992). Half-squaring in responses of cat striate cells. Visual Neuroscience 9, 427–443.CrossRefGoogle ScholarPubMed
Heeger, D.J. (1993). Modeling simple-cell direction selectivity with normalized, half-squared, linear operators. Journal of Neurophysiology 70, 1885–1898.CrossRefGoogle ScholarPubMed
Jagadeesh, B., Wheat, H.S. & Ferster, D. (1993). Linearity of summation of synaptic potentials underlying direction selectivity in simple cells of cat visual cortex. Science 262, 1901–1904.CrossRefGoogle ScholarPubMed
Jones, J.P., Stepnoski, A. & Palmer, L.A. (1987). The two-dimensional spectral structure of simple receptive fields in cat striate cortex. Journal of Neurophysiology 58, 1212–1232.CrossRefGoogle ScholarPubMed
Kontsevich, L.L. (1995). The nature of the inputs to cortical motion detectors. Vision Research 19, 2785–2793.CrossRefGoogle Scholar
Lee, B.B., Elepfandt, A. & Virsu, V. (1981). Phase of responses to sinusoidal gratings of simple cells in cat striate cortex. Journal of Neurophysiology 45, 818–828.CrossRefGoogle ScholarPubMed
Maffei, L., Morrone, C., Pirchio, M. & Sandini, G. (1979). Responses of visual cortical cells to periodic and non-periodic stimuli. Journal of Physiology (London) 296, 27–47.CrossRefGoogle ScholarPubMed
McLean, J., Raab, S. & Palmer, L.A. (1994). Contribution of linear mechanisms to the specification of local motion by simple cells in areas 17 and 18 of the cat. Visual Neuroscience 11, 271–294.CrossRefGoogle Scholar
Movshon, J.A., Thompson, I.D. & Tolhurst, D.J. (1978). Spatial summation in receptive fields of simple cells in the cat's striate cortex. Journal of Physiology (London) 283, 53–77.CrossRefGoogle ScholarPubMed
Poggio, T. & Reichardt, W. (1976). Visual control of orientation behaviour in the fly. Part II. Towards the underlying neural interactions. Quarterly Reviews of Biophysics 9, 377–438.CrossRefGoogle ScholarPubMed
Reid, R.C., Soodak, R.E. & Shapley, R.M. (1987). Linear mechanisms of directional selectivity in simple cells of cat striate cortex. Proceedings of the National Academy of Sciences of the U.S.A. 84, 8740–8744.CrossRefGoogle ScholarPubMed
Reid, R.C., Soodak, R.E. & Shapley, R.M. (1991). Directional selectivity and spatiotemporal structure of receptive fields of simple cells in cat striate cortex. Journal of Neurophysiology 66, 505–529.CrossRefGoogle ScholarPubMed
Tolhurst, D.J. & Dean, A.F. (1991). Evaluation of a linear model of directional selectivity in simple cells of the cat's striate cortex. Visual Neuroscience 6, 421–428.CrossRefGoogle ScholarPubMed
Victor, J.D. (1987). The dynamics of the cat retinal X cell centre. Journal of Physiology (London) 386, 219–246.CrossRefGoogle ScholarPubMed