Abstract
Simple cells in mammalian visual cortex are quasi-linear mechanisms whose behavior departs from true linearity in a very consistent manner. Empirical research on direction selectivity (DS) clearly illustrates these characteristics. A linear DS cell will be DS for all stimuli, whereas a linear non-DS cell will not be DS for any stimuli. However, many simple cells have opposite preferred directions for stimuli of reversed polarity, and some cells are DS for some stimuli (e.g., moving bars) but not for others (e.g., drifting gratings). Also, linear non-DS cells must have separable spatiotemporal receptive fields (RFs), and linear DS cells must have inseparable RFs. Yet many actual DS cells have separable RFs. Here we present a nonlinear model of simple-cell behavior that reproduces all of these empirical behaviors. The model is a variant of the current linear model, amended to include an interleaved nonlinearity (half-wave rectification) that allows it to mimic the (im)balance of push-pull mechanisms. We present simulation results showing that balanced push-pull mechanisms result in linear behavior, while imbalanced push-pull arrangements produce all of the incongruent DS-related behaviors that have been reported for simple cells.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adelson EH, Bergen, JR (1985) Spatiotemporal energy models for the perception of motion. J. Opt. Soc. Am. A 2: 284–299.
Ahmed B, Allison JD, Douglas RJ, Martin KAC (1997) An intracellular study of the contrast-dependence of neuronal activity in cat visual cortex. Cereb. Cortex 7: 559–570.
Berman NJ, Douglas RJ, Martin KAC, Whitteridge D (1991) Mechanisms of inhibition in cat visual cortex. J. Physiol. 440: 697–722.
Bracewell RN (1978) The Fourier Transform and Its Applications. McGraw-Hill, New York.
Carandini M, Anderson J, Ferster D (1998) Membrane conductance changes in simple cells of cat visual cortex (Abstract). Perception, Suppl. 27: 41.
Carandini M, Ferster D (1998) The iceberg effect and orientation tuning in cat V1 (Abstract). Invest. Ophthalmol. Vis. Sci., Suppl. 39: S239.
Carandini M, Heeger DJ (1994) Summation and division by neurons in primate visual cortex. Science 264: 1333–1336.
Carandini M, Heeger DJ, Movshon JA (1997) Linearity and normalization in simple cells of the macaque primary visual cortex. J. Neurosci. 17: 8621–8644.
Casanova C, Nordmann JP, Ohzawa I, Freeman RD (1992) Direction selectivity of cells in the cat's striate cortex: Differences between bar and grating stimuli. Visual Neurosci. 9: 505–513.
Dean AF, Tolhurst DJ (1983) On the distinctness of simple and complex cells in the visual cortex of the cat. J. Physiol. 344: 305–325.
DeAngelis GC, Ohzawa I, Freeman RD (1993a) Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. I. General characteristics and postnatal development. J. Neurophysiol. 69: 1091–1117.
DeAngelis GC, Ohzawa I, Freeman RD (1993b) Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. II. Linearity of temporal and spatial summation. J. Neurophysiol. 69: 1118–1135.
Douglas RJ, Martin KAC, Whitteridge D (1988) Selective responses of visual cortical cells do not depend on shunting inhibition. Nature 332: 642–644.
Emerson RC (1997) Quadrature subunits in directionally selective simple cells: Spatiotemporal interactions. Visual Neurosci. 14: 357–371.
Emerson RC, Citron MC (1992) Linear and nonlinear mechanisms of motion selectivity in simple cells of the cat's striate cortex. In: RB Pinter, B Nabet, eds. Nonlinear Vision: Determination of Neural Receptive Fields, Function, and Networks. CRC Press, Boca Raton. pp. 75–89.
Emerson RC, Coleman L (1981) Does image movement have a special nature for neurons in the cat's striate cortex? Invest. Ophthalmol. Vis. Science 20: 766–783.
Ferster D, Jagadeesh B (1992) EPSP-IPSP interactions in cat visual cortex studied with in vivo whole-cell patch recording. J. Neurosci. 12: 1262–1274.
García-Pírez MA (1998) Reverse correlation analysis and direction selectivity of simple cortical cells (Abstract). Perception, Suppl. 27: 93.
Heeger DJ (1993) Modeling simple-cell direction selectivity with normalized, half-squared, linear operators. J. Neurophysiol. 70: 1885–1898.
Jacobson LD, Gaska JP, Chen H-W, Pollen DA (1993) Structural testing of multi-input linear-nonlinear cascade models for cells in macaque striate cortex. Vision Res. 33: 609–626.
Jagadeesh B, Wheat HS, Kontsevich LL, Tyler CW, Ferster D (1997) Direction selectivity of synaptic potentials in simple cells of the cat visual cortex. J. Neurophysiol. 78: 2772–2789.
Jones JP, Stepnoski A, Palmer LA (1987) The two-dimensional spectral structure of simple receptive fields in cat striate cortex. J. Neurophysiol. 58: 1212–1232.
Livingstone MS (1998) Mechanisms of direction selectivity in macaque V1. Neuron 20: 509–526.
McLean J, Palmer LA (1989) Contribution of linear spatiotemporal receptive field structure to velocity selectivity of simple cells in area 17 of cat. Vision Res. 29: 675–679.
McLean J, Raab S, Palmer LA (1994) Contribution of linear mechanisms to the specification of local motion by simple cells in areas 17 and 18 of the cat. Visual Neurosci. 11: 271–294.
Movshon JA, Thompson ID, Tolhurst DJ (1978) Spatial summation in the receptive fields of simple cells in the cat's striate cortex. J. Physiol. 283: 53–77.
Mullikin WH, Jones JP, Palmer LA (1984) Receptive-field properties and laminar distribution of X-like and Y-like simple cells in cat area 17. J. Neurophysiol. 52: 350–371.
Murthy A, Humphrey AL, Saul AB, Feidler JC (1998) Laminar differences in the spatiotemporal structure of simple cell receptive fields in cat area 17. Visual Neurosci. 15: 239–256.
Reid RC, Soodak RE, Shapley RM (1987) Linear mechanisms of directional selectivity in simple cells of cat striate cortex. Proc. Natl. Acad. Sci. USA 84: 8740–8744.
Reid RC, Soodak RE, Shapley RM (1991) Directional selectivity and spatiotemporal structure of receptive fields of simple cells in cat striate cortex. J. Neurophysiol. 66: 505–529.
Saul AB, Humphrey AL (1992) Evidence of input from lagged cells in the lateral geniculate nucleus to simple cells in cortical area 17 of the cat. J. Neurophysiol. 68: 1190–1208.
Tolhurst DJ, Dean AF (1991) Evaluation of a linear model of directional selectivity in simple cells of the cat's striate cortex. Visual Neurosci. 6: 421–428.
Tolhurst DJ, Heeger DJ (1997) Comparison of contrast-normalization and threshold models of the responses of simple cells in cat striate cortex. Visual Neurosci. 14: 293–309.
Watson AB, Ahumada AJ (1985) Model of human visual-motion sensing. J. Opt. Soc. Am. A 2: 322–342.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
García-Pérez, M.A. Direction Selectivity and Spatiotemporal Separability in Simple Cortical Cells. J Comput Neurosci 7, 173–189 (1999). https://doi.org/10.1023/A:1008924122155
Issue Date:
DOI: https://doi.org/10.1023/A:1008924122155