Orientation sensitivity of ganglion cells in primate retina

Abstract

The two-dimensional shape of the receptive field center of macaque retinal ganglion cells was determined by measuring responses to drifting sinusoidal gratings of different spatial frequency and orientation. The responses of most cells to high spatial frequencies depended on grating orientation, indicating that their centers were not circularly symmetric. In general, center shape was well described by an ellipse. The major axis of the ellipse tended to point towards the fovea or perpendicular to this. Parvocellular pathway cells had greater center ellipticity than magnocellular pathway cells; the median ratio of the major-to-minor axis was 1.72 and 1.38, respectively. Parvocellular pathway cells also had centers that were often bimodal in shape, suggesting that they received patchy cone/bipolar cell input. We conclude that most ganglion cells in primate retina have elongated receptive field centers and thus show orientation sensitivity.

FIGURE 1.

Response of a primate retinal ganglion cell to drifting gratings of different orientations. a, PSTHs of an ON-center MC-pathway cell to a 3-cpd grating drifting at 4.03 Hz. Two cycles of response are plotted. b, Fundamental response amplitude as a function of grating orientation for the gratings in a (filled symbols) and for ones of the same orientation moving in the opposite direction (unfilled symbols). This cell was the only one of five to show a slight directional preference.

FIGURE 2.

Spatial frequency curves of three MC-pathway cells having different orientation sensitivities. The first cell (a) is an ON-center cell, the other two (b-c) are OFF-center cells. Filled and unfilled symbols plot the fundamental response to the gratings depicted to the right. Solid lines are the best fit of a difference-of-Gaussian model (see Methods) to the data.

FIGURE 3.

Spatial frequency curves of three PC-pathway cells having different orientation sensitivities. The first cell (a) is an OFF-center +L-M cell, the other two (b-c) are ON-center +L-M cells. Symbols and lines are the same as in Fig. 2.

FIGURE 4.

Orientation tuning curves of the MC- and PC-pathway cells in Figs. 2 and 3. Grating spatial frequency was 4 cpd for all cells except the cell in Fig. 3a, for which it was 6 cpd. Solid lines are the best fit of a Gaussian function to the data.

FIGURE 5.

Spatial frequency and orientation tuning curves of an ON-center +M-L cell having a bimodal receptive field center profile. a, spatial frequency curves for grating orientations of 22.5 deg (filled symbols) and 112.5 deg (unfilled symbols). b, orientation tuning curves for grating spatial frequencies of 2 cpd (filled symbols) and 3 cpd (unfilled symbols). Solid lines connect points of common orientation (left) or spatial frequency (right).

FIGURE 6.

Receptive field center shape of the MC- and PC- pathway cells in Figs. 2 and 3. Filled symbols plot model estimates of Gaussian center radius from Figs. 2 and 3 for each axis of measurement (0–157.5 deg). The same estimates were used for the opposite direction of motion along a given axis (180–337.5 deg). Solid lines are the best fit of an ellipse to the data. The ratio of the major-to-minor axis of the ellipse, or ellipticity index, was 1.15 (a), 1.49 (b), and 1.76 (c) for the MC-pathway cells and 1.20 (a), 1.70 (b), and 2.16 (c) for the PC-pathway cells. The orientation bias was 0.03 (a), 0.10 (b), 0.14 (c) for the MC-pathway cells and 0.05 (a), 0.16 (b), and 0.25 (c) for the PC-pathway cells. Radial rings are 0.05 deg of visual angle apart.

FIGURE 7.

Orientation selectivity of primate ganglion cell receptive field centers. a, Histogram of ellipticity indices from the ensemble of recorded MC- (filled bars) and PC-pathway (unfilled bars) cells. b, Histogram of orientation bias indices for the two ganglion cell populations. c, Relationship between ellipticity index and bias index of MC- (filled circles) and PC-pathway (unfilled circles) cells. The subset of MC- and PC-pathway cells having bimodal center profiles are identified by dotted symbols. The curve gives the orientation bias index computed for a perfectly elliptical center profile having different ellipticity indices.

FIGURE 8.

Preferred orientation of primate ganglion cell receptive field centers. a, Receptive field locations and center ellipticity of the ensemble of recorded cells. Lines depict the orientation of the major axis of the receptive field center. They are scaled in length in proportion to the ellipticity index (E) of the cell by the equation 2∙(E-1). Small crosshairs mark the location of the fovea. Radial rings are 5 deg apart. b, Ellipticity index of MC- (filled symbols) and PC-pathway (unfilled symbols) cells as a function of retinal eccentricity. The subset of MC- and PC-pathway cells having bimodal center profiles are indicated by dotted symbols. c, Histogram of the absolute angular difference between the preferred and polar angle of cells. Polar angle is the angle formed by a line intersecting the receptive field midpoint and the fovea measured with respect to horizontal. The first bin of the histogram thus gives the number of center profiles that pointed within ±15 deg of the fovea and the last bin gives the number that pointed –75 to –90 deg and 75 to 90 deg of the fovea.

FIGURE 9.

Measures of orientation sensitivity based on response amplitude depend on spatial frequency. a, orientation tuning curves of an OFF-center MC-pathway cell for a 2- (top), 3- (middle), and 4-cpd (bottom) drifting grating. Lines connect points of common spatial frequency. b, Ellipticity index (filled bars) and orientation bias index (unfilled bars) computed at each spatial frequency from response amplitude.